For the Record American Scientist Essays on Scientific Publication Sigma Xi, The Scientific Research Society Research Triangle Park, North Carolina 2011 Sigma Xi, The Scientific Research Society is an international, multidisciplinary research society whose programs and activities promote the health of the research enterprise and honor scientific achievement. Sigma Xi publishes American Scientist magazine, in which these essays originally appeared. Copyright © 2011 by Sigma Xi, The Scientific Research Society, Incorporated. ISBN 978-0-615-55514-0 (paper) Table of Contents Preface Jerome F. Baker 1.Honesty . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 John F. Ahearne 2. A Troubled Tradition . . . . . . . . . . . . . . . . . . . 7 David B. Resnik 3. Authorship Diplomacy . . . . . . . . . . . . . . . . . 15 Melissa S. Anderson, Felly Chiteng Kot, Marta A. Shaw, Christine C. Lepkowski and Raymond G. De Vries 4. Making Ethical Guidelines Matter . . . . . . 25 Michael J. Zigmond 5. Digitizing the Coin of the Realm . . . . . . . . 35 Francis L. Macrina 6. Raising Scientific Experts . . . . . . . . . . . . . . . 45 Nancy L. Jones Bibliography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55 Preface Since its founding in 1886, Sigma Xi, The Scientific Research Society has fostered integrity in engineering and science. The founding members of the Society pledged in the charter to promote and encourage “the highest and the truest advances in the scientific field” and “to lend aid and encouragement” to the newest scientists and engineers. It was with acknowledgment to our rich history that this booklet was conceived. The essays contained in this volume were originally printed in American Scientist, and have contributed to the celebration of Sigma Xi’s 125th anniversary. Two other ethics booklets published by Sigma Xi have played a part in training numerous engineers and scientists for the past 30-plus years. The present volume is intended to build upon Honor in Science and The Responsible Researcher: Paths and Pitfalls. The specific focus on peer review and authorship in this booklet is critical to successfully sharing new scientific knowledge. Authorship helps define who is responsible for study design, data collection and analysis, and interpretation of results. Peer review is the quality-control step in the dissemination of knowledge. For the Record will become a part of Sigma Xi’s efforts to address in a significant way the leadership characteristics of the newest engineers and scientists. Sigma Xi has been fortunate to have Dr. Elsa Youngsteadt working on this project for the past 18 months. Her leadership and commitment have been critical to the booklet’s completion. She has collaborated with the authors and assisted with the editing of each essay. I want to extend a sincere thank you to the authors of the essays for their important contributions and ideas expressed in this booklet. Appreciation is also extended to Katie Lord for her efforts and to Spring Davis for her design assistance. Finally, I offer a special thank you to Dr. John Ahearne for encouraging me and this project. It is our goal that you, the reader, will use these articles to guide your own research and to help you mentor your colleagues and students. Jerome F. Baker, Executive Director and Publisher 1 1 Honesty Ultimately, ethics in scientific publishing, as in life, comes down to one word John F. Ahearne During my 20-year career in the United States capital advising several levels of government on matters of energy and defense, I witnessed many instances of honesty, as well as some of dishonesty, and the consequences of each. Those experiences reinforced my commitment—one held throughout my adult life—to practice the virtue of honesty and to instill it in my colleagues. But even though truthfulness is essential to progress, it is clearly not so easy to uphold. As the Roman poet Juvenal wrote in the first century a.d., “Honesty is praised and then left to freeze.” Touted but not applied. This frailty of human nature, lamented for millennia, clearly has ongoing implications for the progress of both science and society. What Is Honesty? A dictionary definition of honesty belies the rigor and complexity of its practice. According to the Random House description, honesty is: 1. The quality or fact of being honest; uprightness and fairness. 2. Truthfulness, sincerity or frankness. 3. Freedom from deceit or fraud. The commitment required to realize these simple terms is more clearly implied in a second definition, drawn from Funk & Wagnalls Standard Handbook of Synonyms, Antonyms and Prepositions: “One who is honest in the highest and fullest sense is scrupulously careful to adhere to all known truth and right even in thought.” Few would contest the desirability of honesty, and good intentions are nearly universal. As Tina Gunsalus, director of the National Center for Professional and Research Ethics, observes: “Almost everybody wakes up every day and wants to do the right thing.” Later in the day, the goal may be thwarted; the potential pitfalls are many. One might ask, for example, what long-term damage could come from seemingly insignificant transgressions. This reasoning seems to be a common justification among students who cheat on exams, papers and 2Honesty even theses. If such students don’t understand who is harmed, it is hard to convince them that the detriments of deceit outweigh the benefits. Ethicist Sissela Bok, however, warns that “trust and integrity are precious resources, easily squandered, hard to regain. They can thrive only on a foundation of respect for veracity.” Thus small transgressions, if discovered, can easily destroy one’s credibility on a larger scale. And, even if undiscovered, missteps set up the classic “slippery slope” on which small transgressions lead to larger ones. Habits form, and harm is done first to one’s self and then to others. Dishonesty may also take the form of omission, as opposed to overt deception. To address the entire truth without exception can demand extraordinary courage, as United Nations Secretary General Ban Ki-moon has demonstrated. In early November 2010, Ban met with President Hu Jintao of China in Beijing. He discussed climate change, tensions on the Korean peninsula and peacekeeping. However, as the editors of The New York Times pointed out, “He was shamefully silent on one critical issue: China’s poor human rights record and its unjustified imprisonment of Liu Xiaobo, the country’s leading democracy activist and ... winner of the [2010] Nobel Peace Prize.” Ban has many responsibilities, but speaking truth to power is one of them, and in Beijing he was unable to deliver. This is not to say that it is impossible to elevate ethical commitments above the immediate obstacles. In his 1955 book Profiles in Courage, then-Senator John Kennedy emphasized that individuals can rise above their desire for personal advantage and advocate positions that they know are right—even when doing so may damage their careers. Among the courageous figures featured in the book are John Quincy Adams, Daniel Webster, Sam Houston and Robert Taft. Although these men held positions that were often right, they suffered politically for doing so. Robert Taft, for example, was a leading figure in the Republican Party when he gave a speech attacking the Nuremberg Trials of Nazi war criminals. Although he did not support any of the Nazi actions, he concluded that the injustices in the trials were too great to ignore. He was harshly criticized by his party. In today’s political environment of bitter attack ads and communications at the speed of the Internet, such courageous positions can have immediate negative consequences. Perhaps because of that, in recent years principled stands taken by political leaders seldom seem to be positions that could harm their careers. A House of Cards The value of honesty to science is not essentially different from its value to society as a whole, but the progress and application of science do depend fundamentally on the truthful reporting of research. As Nobel John F. Ahearne 3 Laureate Michael Bishop explained to a group of high-school students, “Each of us builds our discoveries on the work of others; if that work is false, our constructions fall like a house of cards and we must start all over again.” This dependency is widely recognized and acknowledged in science and engineering. Consider, for example, the National Academies’ instruction manual for new interns, which states that the “responsible and ethical conduct of research is critical for excellence, as well as public trust, in social science, science and engineering, and is considered essential to the preparation of future scientists and engineers.” In the later decades of the 20th century, examples of scientific misconduct led scientific establishments to formalize ethical guidelines. One such code was published by the National Academies in On Being a Scientist: A Guide to Responsible Conduct in Research. First printed in 1988 and now in its third edition, the booklet clearly addresses the role of honesty and trust in research: The progress and application of science do depend fundamentally on the truthful reporting of research. Over many centuries, researchers have developed professional standards designed to enhance the progress of science and to avoid or minimize the difficulties of research.... Researchers have three sets of obligations that motivate their adherence to professional standards. First, researchers have an obligation to honor the trust that their colleagues place in them.... Second, researchers have an obligation to themselves. Irresponsible conduct in research can make it impossible to achieve a goal.... Third, because scientific results greatly influence society, researchers have an obligation to act in ways that serve the public. A failure to meet these obligations is corrosive to science. As the authors of On Being a Scientist explain: The scientific enterprise is built on a foundation of trust.... When this trust is misplaced and the professional standards of science are violated, researchers are not just professionally affronted—they feel that the base of their profession has been undermined. This would impact the relationship between science and society. Thus a failure to be honest can directly damage the scientific enterprise and can also erode the public’s faith in science. Publication and Temptation Of course, each discipline of science and engineering faces unique ethical challenges, including the humane treatment of research animals and the environmental consequences of engineering designs. But one 4Honesty nearly universal ambition among scientists and engineers at all stages of their careers is publication. In the words of biologist and former editor-inchief of Science Donald Kennedy, “in the world of scholarship, we are what we write. Publication is the fundamental currency; ... research quality is judged by the printed word.” And as stated in On Being a Scientist: The rewards of science are not easily achieved. At the frontiers of research, new knowledge is elusive and hard won. Researchers often are subject to great personal and professional pressures. Authorship is therefore essential for scientists who seek career advancement in academia, industry and government. But the high-pressure obligation to publish may drive some researchers to ethical violations. Triggered by ethical lapses in two prominent physics cases, the American Physical Society (APS) formed a Task Force on Ethics. The team, led by Frances Houle, surveyed all APS members who had completed a Ph.D. within the past three years. The results, published in 2004, were disturbing: 39 percent of respondents said they had personal knowledge of ethical transgressions, the two most common of which were inclusion of inappropriate authors on a publication and exclusion of appropriate authors. One respondent wrote that “many breaches of ethics arise from the pressure to publish.... The recent sad events [show] that it is for many people more important to publish spectacular results than to publish true results.” Physicists are not alone in their difficulties with authorship, the fair assignment of which presents a major and ongoing challenge in all fields of science and engineering that have been surveyed. Abuse of power may lead to the exclusion of deserving authors, and “guest” authorship may be offered to individuals who did not participate substantially in the research. Temptations to cut corners can be great. Among the ethical transgressions involving authorship, perhaps the most egregious are fabrication, falsification and plagiarism. According to the book Responsible Science, “fabrication is making up data or results,” and “falsification is changing data or results.” These usually involve experimental results. Plagiarism does not: It is “the appropriation of another person’s ideas, processes, results or words without giving appropriate credit,” says the Federal Policy on Research Misconduct. Under pressure, some authors maintain honesty and follow the guidelines of science. Some do not. The other side of the publication coin is peer review, a necessary form of quality control that helps ensure the value of a publication. But controversy continues about the fairness and adequacy of the process, and serving as a reviewer can be both an honor and a burden. W. Robert Connor, the former director of the National Humanities Center, summed up the ethical complexity of a reviewer’s task in The Responsible Researcher, a Sigma Xi handbook that I wrote: John F. Ahearne 5 [For] investigators who may find themselves asked to participate in peer review decisions at a relatively early stage in their careers ... there are a host of issues that need to be thought through—how one deals with friends or rivals whose applications may be in the pile, how one deals with approaches and methodologies that may be legitimate but with which one is not sympathetic, how much one can legitimately “borrow” from research proposals one reviews, etc. Clearly, the issues surrounding authorship and peer review are many. Their nuances are discussed further in these pages. At the root of any publication decision, however, should be the basic quality of honesty. Without it, the system of credit, responsibility and quality control in the scientific record is undermined—and the house of cards will fall. Not So Fast The virtue of honesty seems to be under great challenge in the world of blogs, Twitter and television “news” programs. An old saying, often attributed to Mark Twain, identifies the fundamental problem: “A lie can travel halfway around the world while the truth is putting on its shoes.” If only these media were used as often to expose lies and herald truths. Honesty is necessary for science to advance. Unfortunately, it does not seem to be necessary for society’s leaders, the individuals who largely hold the purse strings for science, to practice honesty. Recently, The New York Times columnist Thomas Friedman wrote about this problem: When widely followed public figures feel free to say anything, without any fact-checking, we have a problem. It becomes impossible for a democracy to think intelligently about big issues—deficit reduction, health care, taxes, energy/climate—let alone act on them. Facts, opinions and fabrications just blend together. For the long-term health of the research community and of the individual, honesty is the best policy. John F. Ahearne is an adjunct scholar for Resources for the Future and an adjunct professor of engineering at Duke University. He has served as commissioner and chairman of the U.S. Nuclear Regulatory Commission, system analyst for the White House Energy Office, U.S. Deputy Assistant Secretary of Energy, U.S. Principal Deputy Assistant Secretary of Defense, executive director of Sigma Xi and director of Sigma Xi Ethics Programs. He is a member of the National Academy of Engineering and the American Academy of Arts and Sciences, a fellow of the American Physical Society, the Society for Risk Analysis and AAAS, and chair of the advisory committee of the National Academy of Engineering Center for Engineering, Ethics and Society. He received a Ph.D. in physics from Princeton University. 7 2 A Troubled Tradition It’s time to rebuild trust among authors, editors and peer reviewers David B. Resnik By the mid-1700s, editors at the world’s first scientific journal had a problem on their hands. Since its inaugural issue in 1665, the Philosophical Transactions of the Royal Society of London had published many outstanding scientific papers, including such classics as Isaac Newton’s experiments with prisms. But some authors had begun to submit works of fiction and rambling speculative essays. To maintain standards of quality, the editors of Philosophical Transactions launched a system of peer review to evaluate manuscripts before publication. Two centuries went by, however, before the system really caught on. In the mid20th century, increased specialization, government support for research, and competition for journal space compelled editors to seek assistance from experts. The world’s first scientific journal, the Transactions of the Royal Today, peer review is an essential part Philosophical Society of London, pioneered a system of of scientific publication and is also used peer review to help editors evaluate manuto evaluate manuscripts, grants and scripts. (Image from The Online Books Page, http://onlinebooks.library.upenn.edu.) academic careers. In publication, peer review serves two distinct functions: It ensures that work is published only if it meets appropriate standards of scholarship and methodology, and it helps authors improve their manuscripts. The process begins when authors submit a manuscript to a journal, often with a list of suggested reviewers and a list of scientists who should not see the work. The journal editor sends papers of interest to members of the editorial board or outside experts who review 8 A Troubled Tradition the work for free. These referees assess the manuscript for originality, importance, validity and clarity. They also advise the editor about the manuscript’s overall merit and provide written comments—usually anonymously—for the authors. Finally, the editor decides to publish, reject or request revisions to the manuscript. Although it is hard to imagine how science could progress without independent evaluation of research, peer review is an imperfect system, fraught with questions of bias, efficacy and ethics. At each step of the process, there are opportunities and temptations for reviewers to go astray, and these can take many forms, from simple negligence to intentional abuse for personal gain. If scientific publications are to remain a reliable record of knowledge and progress, editors and reviewers must actively cultivate high ethical standards. The Importance of Trust It seems that most scientists have a story or two about suspected unethical behavior among reviewers. As a beginning assistant professor, I submitted a paper on scientific methodology to a prestigious philosophy journal. The review took a long time—over a year—and when I finally got a decision, the paper was rejected with little comment. A couple of months after that rejection, a paper very similar to mine appeared in the same journal. The article did not plagiarize my work word-for-word, but it defended a similar thesis using many of the same arguments. I suspected that the author had served as a referee for my paper and had delayed his review to prevent my article from being published—or perhaps that he had pilfered my ideas. It is possible that the author of this competing paper had independently arrived at conclusions and arguments similar to mine, and that he had submitted his work to the journal before I did. But I had no way of knowing whether this was so. In the end, I was left with a bitter taste in my mouth, and I lost some trust in the integrity of peer review. It can be hard to determine when a reviewer has abused his or her position. Unscrupulous referees may plagiarize a submitted manuscript, breach confidentiality, delay the review process in order to stifle competitors, use data or methods disclosed in a manuscript without permission, make personal attacks on the authors or require unnecessary references to their own publications. Incidents such as these violate the foundation of trust that is essential to successful evaluation of scientific manuscripts. Authors, editors and reviewers must rely on one another to fulfill their roles with honesty, transparency, confidentiality and professionalism. Absent such trust, the system simply doesn’t work: Authors and editors may ignore reviews that they think are biased or incompetent. Or, fearing that their ideas could be stolen, authors may withhold information necessary to repeat experiments—thereby compromising a key function of scientific David B. Resnik 9 publication. Editors who do not trust reviewers to work carefully and disclose conflicts of interest may ignore their comments or delay publication by seeking other reviewers. Disillusioned reviewers may submit careless evaluations or refuse to review manuscripts. Finally, authors who violate reviewers’ and editors’ trust by submitting fraudulent results can create lasting discipline-wide difficulties for other researchers. To promote trust among authors, editors and reviewers, it is essential that all parties follow ethical standards. Most policies and scholarship related to scientific publication focus on the ethical duties of authors, but at least two sets of important guidelines do address reviewers. The International Committee of Medical Journal Editors recommends that peer review be unbiased and that journals publish their peerreview policies. The Committee on Publication Ethics (COPE), a nonprofit organization of journals, publishers and individuals, has developed guidelines that address confidentiality of peer review, protection of intellectual property, fairness and conflict-of-interest management. Some standards of peer review for editors and referees, recognized by COPE and leading authorities on research integrity, are: Confidentiality: Maintain confidentiality throughout the review process. Respect for intellectual property: Do not use authors’ ideas, data, methods, figures or results without permission. Fairness: Avoid biases related to gender, nationality, institutional affiliation and career status. Professionalism: Read manuscripts carefully, give constructive criticism, avoid personal attacks and complete reviews on time. Review only manuscripts that you are qualified to review. Conflict-of-interest management: Disclose personal, professional or financial interests that could affect a review and avoid reviewing an article if a conflict of interest could compromise judgment. If referees followed these guidelines faithfully, I suspect there would be very few setbacks in peer review. Problems Despite efforts to encourage professionalism among reviewers, troubles persist. One of the best-documented issues is inefficacy: Reviewers may miss errors, methodological flaws or evidence of misconduct. To measure reviewers’ ability to catch errors, Magne Nylenna of the Journal of the Norwegian Medical Association and his colleagues created two inauthentic manuscripts with obvious methodological flaws such as inappropriate statistical tests. They sent the papers for review and graded reviewers on the number of flaws they caught. The average score was only 1.7 out of 4, and more than one-third of the reviewers provided no comments on methodology at all. Nylenna’s results were not anomalous. In a similar study led by Fiona Godlee of the British Medical Journal, 10 A Troubled Tradition reviewers discovered, on average, only 2 out of 8 errors introduced into manuscripts. These studies did not determine why reviewers missed so much, but they may have simply read the manuscripts carelessly. Falsification and fabrication are problems that reviewers shouldn’t have to worry about—but in reality, they must remain alert. One of the most famous examples occurred in 2004 and 2005, when South Korean researcher Woo-Suk Hwang and colleagues published two papers in Science claiming to have developed human embryonic stem-cell lines that were genetically identical to patients’ cells. The work would have been a breakthrough in regenerative medicine, but in June 2005, a whistleblower declared that some of the data were fake. Eventually, a university investigation found that Hwang had fabricated data in both papers, which were then retracted. Whether editors and reviewers should have spotted evidence of Hwang’s misconduct is unclear—but without access to raw data, detecting fraud is notoriously difficult. Indeed, the incident prompted the editors of Science to scrutinize high-profile papers more closely, requiring authors to provide original data and examining digital images more carefully. Even when reviewers do catch flaws in a manuscript, they may not all agree in their assessments. In one recent study, Richard Kravitz of the University of California, Davis, and colleagues examined reviewer recommendations for more than 2,000 manuscripts submitted to the Journal of General Internal Medicine. For editors to publish work with confidence, reviewers ideally should agree about whether to accept or reject a manuscript—but in fact, they concurred only slightly more often than if they had made their decisions by coin toss. Multidisciplinary research can cause particular confusion because reviewers from different disciplines may accept different methodological standards. In these cases, editors may feel the need to seek additional reviews, potentially delaying publication. A more subtle but equally pervasive problem is reviewer bias. A reviewer’s evaluation can be influenced by an author’s institutional affiliation, nationality, gender or career status, or by the reviewer’s own financial or professional interests. For example, a referee might be more likely to give a favorable review to a friend than to a competitor, or to favor a well-known researcher from a prestigious institution over a less-familiar researcher. Although specific allegations of bias are difficult to prove, the phenomenon has been documented in systematic studies. In a 1982 study, for example, Douglas Peters and Stephen Ceci selected 12 previously published psychology papers by authors from prestigious institutions, then resubmitted the papers to the same journals using fake author names and institutions. Of nine journals that sent the papers for review, eight rejected them due to poor quality. The results suggest that the original reviewers’ favorable evaluations may have been influenced by the prestige of the authors or their institutions. Although the sample David B. Resnik 11 incompetent biased unnecessary references personal attacks delayed review breached confidentiality used ideas, data, methods without permission 0 10 20 30 40 50 survey responses (percent) 60 70 80 Biomedical researchers at the National Institute of Environmental Health Sciences have experienced an array of ethical problems with peer review. Well over half of those surveyed in 2006 said they had received at least one biased or incompetent review. More malicious ethical problems, such as breach of confidentiality, were also disturbingly common. (Illustration by Barbara Aulicino.) size was small and the experiment lacked controls, larger trials with alternative forms of peer review also suggest that referees are influenced by their assumptions about authors. More malicious transgressions, such as intentionally delaying reviews, are less well documented. To fill this gap in the literature, my colleagues, Shyamal Peddada and Christine Gutierrez-Ford, and I conducted a survey in 2006 to ask scientists about a range of problems in peer review. The respondents included 220 postdoctoral researchers, staff scientists, principal investigators and technicians working in 22 different biomedical disciplines at the National Institute of Environmental Health Sciences (NIEHS). They were about 54 percent male and 44 percent female; 2 percent did not specify gender. On average, they were 42 years old and had about 35 publications each. Reviewer incompetence was the most common problem this group reported: More than 60 percent of respondents said they had encountered at least one reviewer who did not read an article carefully, was not familiar with the subject matter or made mistakes of fact or reasoning in the review (see the chart above). About half said a reviewer was biased. Other common problems were that reviewers required unnecessary references to their own publications or made personal attacks in reviews. About 10 percent of respondents said a referee delayed the review so that he or she could publish an article on the same topic. Rarer, but still troubling, were reports that reviewers had breached confidentiality or used ideas, data or methods without permission. An author’s age and number of publications were both positively associated with experiencing an incompetent or biased reviewer—perhaps because a researcher who has published more papers has had more opportunities to encounter reviewers whom he or she views as biased or incompetent. Scientists who are well established in a field may also be less 12 A Troubled Tradition open to criticism from reviewers and therefore be more likely to perceive reviews as inadequate. This study did have some limitations. The questionnaire asked for respondents’ experiences, but we did not attempt to confirm whether alleged problems actually occurred. For example, some reports of reviewer bias might simply reflect the authors’ dissatisfaction with a referee’s comments. We also did not attempt to determine how frequently respondents experienced the problems they reported. Finally, our sample of biomedical researchers working at a government institution may or may not reflect the experiences of other researchers at other institutions or in other disciplines. The study does, however, provide some of the only empirical evidence that scientists regularly experience a range of ethical problems with peer review. To expand upon our results, future research should examine the prevalence and significance of such problems in peer review, as well as potential causes—such as inadequate training, or competition for status or funding. This research might take the form of focus groups, interviews and surveys with editors, reviewers and authors. The results could guide both policy development and educational initiatives. Alternative Forms of Peer Review Some journals and conferences have adopted or tested alternative forms of peer review. One common alternative, double-blind review, could serve to reduce reviewer bias because neither authors nor reviewers know each other’s identities or affiliations. Another alternative is unblinded (or open) review, in which both authors and reviewers do know each other’s identities—a situation that might encourage ethical behavior among reviewers who cannot hide behind a cloak of anonymity. Studies of these two forms of review have, however, yielded mixed results. Logistics are an important hurdle: In trials of doubleblind review, several medical journals found that about one-quarter to one-half of reviewers were able to correctly guess authors’ identities despite blinding. And in trials of open review, referees who were asked to reveal their names to authors often refused to participate. There is nevertheless evidence that blinding does reduce bias. Joseph Ross of the Robert Wood Johnson Clinical Scholars Program led a five-year study, published in 2006, which showed that authors’ nationality and institutional affiliation affected acceptance of abstracts for the American Heart Association’s annual Scientific Sessions. Among thousands of abstracts submitted per year, blinded reviewers accepted about 12 percent fewer abstracts from prestigious institutions than did reviewers who were aware of authors’ affiliations. Blinded reviewers also accepted fewer abstracts from within the United States and more David B. Resnik 13 from outside the United States than did unblinded reviewers. Blinding must have reduced bias resulting from reviewers’ assumptions about authors’ countries and institutions. Whether blinding also improves the quality of reviews is unclear. In 1990, Robert McNutt and colleagues found that blinded reviewers provided more accurate, well-supported and courteous reviews than did unblinded reviewers of articles submitted to the Journal of General Internal Medicine. But several years later, Amy Justice led a similar study with five different medical journals, and found no effect of blinding on review quality. Results for open review have been similarly mixed. One study at the British Journal of Psychiatry, led by Elizabeth Walsh, found that when referees revealed their identities to authors, they provided better reviews, were more courteous, took longer to complete reviews, and were more likely to recommend publication than were anonymous reviewers. But a pair of studies led by Susan Van Rooyen of the British Medical Journal found that revealing reviewers’ identities—either to authors or to co-reviewers—did not impact review quality or reviewers’ recommendations. The discrepancies among these studies of double-blind and open review could arise from their differing methodologies and sample populations. It is also worth mentioning that none of these studies examined the most serious ethical issues, such as respect for intellectual property. Future studies should take these factors into account, and they may eventually tip the balance in favor of one form of review or another. Conclusion Peer review is a key feature of scientific publication, but it is susceptible to bias, inefficacy and other ethical transgressions. Alternative forms of review have produced only equivocal improvements in fairness and efficacy and have not been tested with respect to other problems. What are the next steps we should take to improve peer review? First, researchers should receive more education on how to review scientific articles—a skill that is not typically emphasized during research training. Some scientists do show students and postdocs how to review papers, and some research institutions cover peer review in seminars and workshops on research ethics. These practices must become more widespread. In particular, investigators should teach their trainees how to evaluate articles for scientific merit and to follow ethical standards of peer review. Asking young scientists to help review papers is a good way to educate them, provided journal editors give their permission and the process remains confidential. Journals should also develop and publicize instructions for new reviewers and policies for reviewers and editors, just as they have done 14 A Troubled Tradition for authors. Rules should address confidentiality, fairness, conflict of interest, respect for intellectual property, and professionalism. Editors should carefully manage the peer review process to prevent or address problems and concerns. They should explicitly inform reviewers about their journals’ peer-review policies, remind reviewers to disclose conflicts of interest and return their reports on time, and delete any personal attacks from reviewers’ comments. If editors have evidence that a reviewer provided a poor review or abused the process, they should not invite that person to do other reviews. These ideals may be complicated when editors have difficulty finding experts willing to review a manuscript, and when referees submit their reviews late, overlook errors, or disagree about the quality of a submission. Workshops and conferences on the subject could help editors to cope with these challenges. Finally, scholars should conduct additional research on the ethics of peer review. Our exploratory study of the experiences of NIEHS researchers suggests that some problems are common, but the results should be confirmed in other settings. Future work should determine how often ethical problems occur and how they affect scientists’ attitudes and behaviors. Studies should also address the causes of unethical behavior in journal peer review and the effectiveness of alternatives, such as double-blind or open review, at preventing various types of transgressions. There is certainly no perfect solution to the problem of quality control in the scientific record. Despite its flaws, the system adopted by the editors of Philosophical Transactions two and a half centuries ago seems to work as well as any method that has been tried—but its age and pervasiveness must not foster complacency. While journals, editors and scholars work to understand and regulate peer review, it’s up to every individual scientist to maintain a thoughtful awareness of his or her participation in the process. Such vigilance and professionalism can only improve the quality of reviews, and might even spark new insights into how the review system could eventually be improved. David B. Resnik is a bioethicist at the National Institute of Environmental Health Sciences. He received a Ph.D. in philosophy from the University of North Carolina, Chapel Hill, and a J.D. from the Concord University School of Law in Los Angeles in 2000. Acknowledgments I am grateful to Bruce Androphy, Zubin Master, Christine Flowers and Adil Shamoo for helpful comments. This essay does not represent the views of the NIH, the NIEHS or the U.S. government. 15 3 Authorship Diplomacy Cross-national differences complicate allocation of credit and responsibility Melissa S. Anderson, Felly Chiteng Kot, Marta A. Shaw, Christine C. Lepkowski and Raymond G. De Vries Among scientists, authorship is a very big deal— and for good reason. It not only establishes the record of scientific progress but also stakes a scientist’s claim to originality and priority. As sociologist Robert Merton noted decades ago, recognition for original work is the coin of the realm in science. Authorship is the basis for promotion, tenure, salary, honors and invitations to participate in prestigious initiatives. It is important for collaborating authors to get it right. Getting it right seems like a simple and straightforward task: Include those who contributed to the project and omit those who did not. Most scientists, however, have encountered situations in which coauthors disagreed about who should be included on a publication or in what order they should be listed. In a recent study, two of us and our colleague Brian Martinson found that 12 percent of midcareer scientists admitted that they had inappropriately assigned authorship credit within the previous three years. Such situations may reflect competitive pressures in science or disputes among authors. Problems with authorship are complicated enough in domestic research, but they can be particularly thorny in the context of international scientific collaborations. Whether authorship disagreements are more common in international or domestic research is an open question, but some aspects of cross-national collaboration do complicate authorship decisions. International Collaborations Scientific research is increasingly international in scope and practice. Worldwide, the percentage of science and engineering research articles with authors from more than one country increased from 8 percent in 1988 to 22 percent in 2007, according to the 2010 Science and Engineering Indicators compiled by the U.S. National Science Foundation. 16 Authorship Diplomacy Rates of international collaboration as defined in the Indicators are 20 to 30 percent in the United States, China, Japan and India, but around 50 percent in the European Union, in part because recent EU policies and incentives favor international collaboration. As we consider authorship issues that arise in these collaborative ventures, we draw on our own and our colleagues’ work in the recently published book International Research Collaborations: Much to be Gained, Many Ways to Get in Trouble and our ongoing research on international scientific collaborations. Specifically, we use material from 10 focus groups and 60 interviews that we conducted over the past year with scientists in the U.S. (and a few outside the U.S.) who are involved in cross-national research collaborations. When we asked these scientists about problematic and beneficial aspects of international research, we inevitably heard about issues with authorship and publication. Getting it right seems like a simple and straightforward task: Include those who contributed to the project and omit those who did not. Errors of Omission One of the most obvious problems in collaborative authorship is omitting authors from a paper. The classic form of omission occurs when two collaborators are in conflict (professional or personal) and one leaves the other’s name off a paper out of spite. Such cases are possible in almost any collaboration—domestic or international. But other forms of omission are more directly linked to cross-national research. Qualifications for authorship, based on scientific contribution or professional status, differ internationally. One scientist told us about working with collaborators in another country who were unwilling to give authorship credit to graduate students simply because of their junior status. He tried to correct the injustice without triggering professional retaliation against the students: “You really almost have to be subversive to help younger people in a way that doesn’t ruin their lives at home, which is not so simple—but I think it is a huge integrity issue.” We also heard about researchers who left others’ names off publications in order to advance their own careers. In some countries, a senior scientist may feel entitled to take full credit for a junior colleague’s work. But the reverse can also happen: Sometimes young scientists train in labs outside their native countries, then publish the results on their own once they return home. Authors who are omitted without having given their consent often feel wronged, but sometimes authors agree to be left off a publication Anderson, Kot, Shaw, Lepkowski and De Vries 17 In this map of research collaborations, coauthors’ cities are connected by white lines. The brightness reflects both the number of collaborations between a pair of cities and their proximity. The network is based on author affiliations on scientific papers aggregated in Elsevier’s Scopus database from 2005 to 2009. (Image courtesy of Oliver Beauchesne, Science-Metrix, with adaptations by Tom Dunne.) in exchange for some other form of compensation, usually financial. This arrangement, known as ghost authorship, is a problem in the U.S. as well as in other parts of the world. In 2010, Shen Yang of Wuhan University in China released estimates that Chinese academics spent more than $145 million on ghostwritten papers in the previous year. That sum is considerable, especially considering reports of low pay to ghostwriters. For example, Associated Press reporter Gillian Wong in 2010 wrote about a Chinese ghostwriter who received the equivalent of $45 per paper for composing professors’ research articles. One of our focus-group participants commented that pressures and financial rewards for publications increase Chinese academics’ willingness to pay for ghostwriters. Authors may also remove themselves—either voluntarily or under pressure—from a publication because they fear repercussions for having participated in politically or religiously sensitive research. International collaborators whose research findings may embarrass their governments—for example by exposing weaknesses in healthcare systems—sometimes ask to be omitted from publications for the sake of their careers. Undeserved Credit An omitted author is clearly denied the recognition he or she deserves, but the addition of undeserving authors can also be damaging. Extra names dilute the credit allocated to deserving authors and obscure responsibility for the work. We identify four categories of the addedauthor problem, distinguishing them according to the motivations for 18 Authorship Diplomacy adding an author. These categories overlap to some extent because motivations can be multiple and may not be fully known. Surprise authorship is when a researcher finds out after publication that his or her name appears on a paper. In some cases, collaborators from different countries do not observe the same practices with regard to coauthorship and review of manuscripts. One scientist told us about a paper published by international colleagues: “I found it by stumbling across the paper in the literature. There it is. This is my name, and there’s the paper, and I have never seen this paper. ” Gift authorship occurs when someone is given more credit on a paper than he or she deserves. Sometimes a principal investigator decides that it is someone’s turn to be on a publication and arranges for that person’s name to appear—even if he or she has not done enough to deserve authorship. In other cases, a senior researcher may decide that his collaborators need publications more than he does, so he allocates publication credit generously (or overly generously) to his collaborators. For instance, in some countries it is common practice to include individuals who have only had administrative oversight. One scientist we interviewed complained about too-liberal inclusion standards among his international colleagues: “Sometimes I am very strict about them, basically saying that I’m not going to allow it. Other times I know there is a political reason why they do it, and so unfortunately I may just let it go by.” Gift authorship is less benign when it involves an expected quid pro quo in the form of future assistance, favors or advantages. Honorary authorship is often equated with gift authorship, but the motivations are different. Honorary authorship goes to individuals with higher status, as a way of honoring them personally or in their roles as superiors. One scientist told us about working with collaborators in Europe for whom it was standard practice to include “out of respect” the student, the supervisor, the supervisor’s mentor and the department chair. Often, however, the honor bestowed through unearned authorship is not freely given; rather, it is demanded by supervisors, administrators or funders. This issue came up frequently in our interviews and focus groups. An epidemiologist told us, People may find that in an international context, if there is a head of the laboratory, that person may expect to go on anything regardless of their contribution or lack of contribution.… So there are issues of sensitivity of where somebody is in terms of the hierarchy. A focus-group participant explained: The culture is different. You may be dealing with a researcher who in fact has several layers of bosses. And when it comes to negotiating the dollars, they all get involved. When it comes to publications, they all get to have their name on the paper. Anderson, Kot, Shaw, Lepkowski and De Vries 19 50 international coauthorship (percent) 45 European Union 40 35 30 China 25 Asia (8 countries) 20 India United States 15 10 Japan 5 0 1989 1991 1993 1995 1997 1999 2001 2003 2005 2007 year Articles with authors in two or more countries represent the fastest-growing segment of the science and engineering literature. European Union incentives that encourage collaboration within Europe have had a striking effect. The eight Asian countries represented by the dotted line are India, Indonesia, Malaysia, the Philippines, Singapore, South Korea, Taiwan and Thailand. (Illustration by Tom Dunne, adapted from data published by the U.S. National Science Board.) In a 2010 Nature article, author Karen Kaplan relayed suggestions from academics on how to get tenure—including “name a senior department member as a coauthor on your papers if you’re in Europe.” In legitimizing authorship, a guest author may be listed because of the credibility that his or her position or status will bring to the publication. As one of our respondents put it, People really want to have your name on their paper, sometimes on papers where you … didn’t even know that they were doing the study. But they’re using a little bit of the reagent you gave them which, you know, you would give anyone freely.… I think that they want your name on a paper because it may legitimize things. Another biomedical scientist told us about her experience of being named an author of a paper by a research group in another country, to which she had sent plasmids. She thought the study was done 20 Authorship Diplomacy incorrectly, and the findings directly contradicted a paper she had published. She continued, They were upset because what they wanted was my name on the paper so that they could submit it to a journal that was a little bit higher up in the hierarchy, because I already had a reputation in the field. So … this was very uncomfortable because I was saying to them, “No, your work isn’t good enough.” And I was trying to find ways not to say that, but that’s frankly what I felt. In other cases, legitimizing authorship comes into play when an author is added to mask the illegitimate contributions of others. For example, pharmaceutical firms may recruit researchers to serve as figurehead authors of company-authored papers in order to hide potential conflicts of interest. The figurehead is usually paid well to allow his or her name to appear, frequently replacing the actual authors who may be acknowledged in a footnote or may be absent altogether. Out of Order Trouble can also arise as collaborators work out the sequence in which their names will appear on a publication. Disciplinary customs differ, particularly in the significance of the first- and last-named authors. Cross-national teams are often cross-disciplinary as well, and the order of authors can be a point of dispute. One of our focus-group members described collaborating with a high-ranking scientist in another country who insisted on taking the last position to signify, he said, his minimal role on the project. In the journal in question, however, the last position indicated a significant responsibility as the corresponding author for the study. The scientist described it as “a very difficult situation.” Another scientist we interviewed had worked with a team that included a member of a royal family (a princess) who expected to be the first author on every publication in her country, regardless of her contribution. Some collaborative teams adjust the order of authors to share credit fairly among themselves. They may adopt alphabetical ordering and rotate the alphabetical list in subsequent papers to take turns being first author. Some teams include a note that all authors, or some subset of the authors, contributed equally. Others take advantage of differences in how contributions are measured in different countries. For example, a biological chemist told us, It worked out nicely.… I was offering them either first or last [author position], thinking that they would of course choose last, but they wanted first, which was perfectly fine with me. That put me last, so in that sense, yeah, it was great. Anderson, Kot, Shaw, Lepkowski and De Vries Plagiarism 21 Recent media attention to plagiarism has alerted scientists to the need to check manuscripts for plagiarized material using increasingly sophisticated software. Plagiarism stakes an implicit authorship claim on someone else’s words or ideas. Recent media attention to plagiarism has alerted scientists to the need to check manuscripts for plagiarized material using increasingly sophisticated software. Plagiarism among international trainees has long been a concern in many countries. In a 2011 article, research ethicists Elizabeth Heitman of Vanderbilt University and Sergio Litewka of the University of Miami Miller School of Medicine discussed numerous factors that may lead to plagiarism. These include the “normalcy of plagiarism” in some social and cultural environments, vague integrity standards, and rejection of U.S. concepts of originality and intellectual property. Plagiarism may also be a strong temptation for international trainees who have difficulty writing in English but are under pressure to publish in English-language journals. Such problems are not unique to students. In a letter published in Nature in 2007, Turkish physicist Ihsan Yilnaz writes, For those of us whose mother tongue is not English, using beautiful sentences from other studies on the same subject in our introductions is not unusual.… Borrowing sentences in the part of a paper that simply helps to better introduce the problem should not be seen as plagiarism. Even if our introductions are not entirely original, our results are. Cultural perspectives on authority also influence writers’ attitudes toward plagiarism. One of our interviewees said, “It took me some years to figure out that there’s an idea at large that anything that comes from authority figures is held in high regard.” She noted that material in the published literature is assumed to come from a person of authority, so students may conclude, “What right do I have to change that person’s words?” Ready access to articles online has made plagiarism easier. Environmental engineer James Leckie observed in an interview that students in some cultures do not believe they are doing anything wrong when they plagiarize. They argue that “if the authors didn’t want you to use their material, they wouldn’t publish it, but since it’s published and accessible, it should be free for everyone to use in any way.” A specific issue in the global context is translation plagiarism—that is, translating a publication in whole or in part and publishing the translation as one’s own work without acknowledging the original authors. One U.S. biomedical researcher we interviewed encountered this 22 Authorship Diplomacy problem with a collaborator in a developing country. The collaborator asked him to review and endorse a book manuscript, which turned out to be a translation of materials that the U.S. researcher had given to the collaborator, for which the collaborator intended to take sole credit. The U.S. scientist saw that the country in question would derive great value from having the materials in its native language, but he confronted the collaborator about the plagiarism: I said, “I’ve got a real problem with this, because I recognize why you’ve done it and all of this, but the fact is that you have put your name on other people’s words, and what you did is you translated it.” And he said, “Well yes!… What’s the problem with that? And aren’t I your friend? And look at what I have done for you!” and things like that. It was pretty awkward. Skills for the Global Context Authorship sits at the intersection between collective effort and individual ambition. Scientists participate in international collaborations for many reasons, including a belief that collaboration will benefit all involved. But the pursuit of individual recognition cannot be completely eliminated. Collaborators must pay careful attention to authorship in order to share credit and responsibility fairly among all team members. The most helpful way to deal with authorship issues is to agree on general principles for authorship at the beginning of the collaboration and then to agree on authorship of each article when its content is first outlined. A U.S. scientist who is experienced at international collaboration told us, “You have to have the guts to tackle [authorship issues] before you go into it.” Another said, I found it difficult at first. But it was very clear that if there is any doubt as to how authorship—especially credit—is going to be divvied up, it is better to approach that before, rather than after, just so everybody has a pretty good idea. It is clear, though, that discussions alone will not clear away all authorship problems. Several resources provide additional guidance. Collaborators should consult the policies of the journals to which they plan to submit their work. International guidance is available through the Council of Science Editors, the Committee on Publication Ethics and the International Committee of Medical Journal Editors’ Uniform Requirements for Manuscripts Submitted to Biomedical Journals. The Singapore Statement, released in conjunction with the Second World Conference on Research Integrity in 2010, provides a succinct statement that responsible authorship is a duty of researchers worldwide. Scientists can join AuthorAID, a free, international research community that supports researchers from developing countries with services such as networking and mentorship. Anderson, Kot, Shaw, Lepkowski and De Vries 23 The U.S. scientists we interviewed were aware of the ethical complexity of authorship and the importance of meeting high standards in practice. But they were also careful to take their collaborators’ perspectives into account. A focus-group participant said, the problem is that our ignorance of the way these kinds of systems work in other countries can sometimes be really detrimental to the way the research is performed and expressed and published. Leckie provides a cautionary example, drawn from his own experience working with an Asian collaborator: I once was designing a research activity with this fellow, and he brought to me very early on several drafts of his part of the proposal. And on it, he had the name of a division head who was associated with the overall program but had nothing to do with his research activity. The division head had no expertise relevant to the proposal and was not going to contribute anything. I told my collaborator, “Look, that guy’s not doing anything. Take his name off.” And he said, “Well, I can’t.” Then I said, “Well then, take my name off.” And so we had a real confrontation, and in the end my collaborator took the name off, and it resulted in an attempt to fire him. Maintaining the integrity of authorship is complicated in the global context, but the stakes can be high for all concerned. It is worth the time and effort required to get it right. Melissa S. Anderson is a professor of higher education in the Department of Organizational Leadership, Policy and Development at the University of Minnesota, Minneapolis. She received a Ph.D. in higher education from the University of Minnesota. She studies research integrity and international scientific collaboration. Felly Chiteng Kot is a Ph.D. candidate and Marta A. Shaw and Christine C. Lepkowski are Ph.D. students in Anderson’s department. Raymond G. De Vries is a professor of bioethics at the Center for Bioethics and Social Sciences in Medicine at the University of Michigan. He received a Ph.D. in sociology from the University of California, Davis. He is writing a social history of bioethics and researching the internationalization of ethics guidelines. 25 4 Making Ethical Guidelines Matter Professional societies are uniquely positioned to develop effective codes of conduct Michael J. Zigmond Back in 1995, I thought it would be a fairly simple job to draft a set of guidelines for the responsible communication of scientific results. The Society for Neuroscience (SfN) wanted such guidelines, and I chaired the committee that drafted them. At first, we assumed that a small group of people would easily prepare a simple document of a few pages. The reality proved to be quite different: The process spanned more than three years, during which our text evolved from a few paragraphs written by two people to about 5,000 words written by a committee of seven, and finally to 13,500 words composed by 13 individuals with experience in academia, industry, publishing and law. Illustration by Tom Dunne. 26 Making Ethical Guidelines Matter Societies are often in the best position to understand and set standards of conduct for the specific segment of science that they represent. In the end, our guidelines didn’t just give instructions; they explained the reasons that researchers should behave in certain ways. And in generating those explanations, we sometimes decided to modify the very rules we had set out to justify. The SfN continues to refine its guidelines today, and the process has stimulated much reflection on the role of professional societies in establishing ethical guidelines—and keeping them alive, relevant and effective. Getting Specific Professional societies have a long and honorable history, tracing back at least to the 15th century. But only very recently have scientific societies begun to establish guidelines on research ethics for their members. Today, more than 50 societies have written guidelines, and this is as it should be: Professional organizations are in a unique position to promote the responsible conduct of research. Responsibility for overseeing research ethics has typically fallen to research institutions rather than societies. But institutions can set standards only for the most basic and universal matters, such as plagiarism and fabrication of data. Other aspects of research, including authorship, data management and the sharing of reagents, can be too specific to a given field to be regulated at the institutional level. True, professional societies are generally ill equipped to investigate claims of misconduct. They also have limited powers of enforcement and few penalties to impose on those who misbehave. But societies are often in the best position to understand and set standards of conduct for the specific segment of science that they represent. Moreover, although there are some 2,500 colleges and universities in the United States alone, there are far fewer scientific societies—each of which can efficiently communicate with a large number of scientists. Finally, societies are increasingly involved in publishing research journals and organizing conferences at which scientists present results. In such venues, these organizations have a unique opportunity—and an obligation—to educate their members about responsible conduct. Integrity in Neuroscience My own work developing guidelines for professional conduct is almost solely with the SfN. But my experiences may illustrate how other societies could begin such an endeavor, what they might do once guidelines are adopted, and what problems they might encounter. The Michael J. Zigmond 27 Ethics discussions such as this one are an integral component of the professional skills workshops that the Society for Neuroscience offers at its annual meetings. (Copyrighted photograph by Jeff Nyveen, courtesy of the Society for Neuroscience, 2010.) SfN example also illustrates how a society can go beyond guidelines alone to promote research integrity in other dynamic ways. The SfN is a relatively young society. The word neuroscience itself did not even appear in the literature until the 1960s, and the SfN was created in 1969. Since then, both the field and the society have expanded rapidly. Indeed, during the past five years, a quarter of a million research articles on aspects of the nervous system were published. That amounts to more than 100 papers every day! And the size of SfN membership has expanded dramatically since its inception, growing from a few hundred to more than 40,000 members. Shortly after its inception, the SfN began to take on ethical issues. In the early 1980s, public concern arose over the treatment of monkeys at the Institute for Behavioral Research in Silver Spring, Maryland. In response, the SfN organized a symposium on the use of animals in research, established a standing committee on the treatment of laboratory animals and human subjects, and developed a formal policy on those issues. The society also established a general policy on research ethics and an initial statement about fabrication, falsification and plagiarism, which was replaced in 1999 with a comprehensive set of guidelines for responsible conduct in scientific communication. Also in the early 1980s, the SfN began to offer a Social Issues Roundtable at the society’s annual meetings. Sessions have included “Neuroscience in Developed and Developing Countries: Partnership or Exploitation,” “Perspectives on Gender in Neuroscience” and an overview of several other ethical issues. The series continues today and adapts to encompass timely issues. Shortly after the destruction of the World Trade Center towers, for example, the program committee abandoned the intended topic in favor of a special session on the impact and treatment of trauma. As another addition to the SfN meetings, my colleague Beth Fischer and I began in 1997 to hold annual workshops on professional skills such 28 Making Ethical Guidelines Matter as writing research articles and making oral presentations. We firmly believe that research ethics are best taught in the context of other skills rather than in isolation, and our workshops adhere to this principle. Skillcentered events tend to attract more students than those that address integrity alone. And where better to discuss authorship criteria and plagiarism than in a workshop on writing research articles? We use the lunch hour for case discussions led by neuroscience faculty members, thereby emphasizing that ethical concerns are worth the time of working scientists. And we establish a supportive culture by acknowledging that students and researchers do need guidance in professional skills that they might not learn in traditional training programs. Melissa Anderson, a social scientist at the University of Minnesota, and her colleagues have shown that such a culture fosters research integrity. To use the words of Addeane Caelleigh, former editor of Academic Medicine, we provide a “hidden curriculum” by presenting a “message of actions rather than formal statements.” The twin objectives of educating and promoting a culture of responsible conduct also led the SfN to establish in 2003 the ongoing annual Neuroethics Lectures. At the most recent lecture, Henry Greely spoke of the many ethical issues raised by discoveries in neuroscience. Among the difficult questions he addressed were: If we develop cognitive enhancers, should they be available to anyone or only to those with special needs? And should we try to detect neurological diseases before symptoms appear even when there are no treatments? At the same meeting, the SfN held a special session called “The Brain on Trial,” in which neurologists testified before an actual judge about whether a fictitious individual should be convicted of murder despite evidence in his brain scans. In 2006, growing interest in the intersection of neuroscience and ethics spawned a whole new organization, now named the International Neuroethics Society. It coordinates its meetings with those of the SfN and hosts symposia on topics such as global health, predictive biomarkers for disease, and neuroscience and national security. Starting from Scratch It was in the context of these expanding ethics initiatives that the SfN decided to develop guidelines on responsible conduct in communicating scientific results. The stimulus for this committee, which I chaired, was a concern among some society members that a few journals were fast tracking papers—that is, soliciting and then prioritizing certain papers rather than evaluating manuscripts in the order in which they were submitted. But the scope of our committee quickly expanded. It is often said that one should not reinvent the wheel, and scientists often (but not always) examine what other people have written about a topic before initiating research in that area. Of course, learning too much about what has already been done can close one’s mind to Michael J. Zigmond 29 new possibilities. At least that is the committee’s excuse for the fact that when we started working on our guidelines, we were not hampered by knowledge! (For those embarking on the task anew, I would now recommend doing a little homework. This might include examining existing guidelines and reading “Eighteen Rules for Writing a Code of Professional Ethics,” by Michael Davis, a philosopher at the Illinois Institute of Technology. Caelleigh’s “Roles for Scientific Societies in Promoting Integrity in Publication Ethics” is another excellent resource.) We did eventually make considerable use of the pioneering efforts of the American Chemical Society, which kindly gave us permission to adapt and extend its guidelines for our purposes. We might also have begun by considering our objective: How did we want our guidelines to be used? Mark Frankel, a senior staff member of the American Association for the Advancement of Science, has been a major force in encouraging professional societies to promote research integrity. He has noted that codes of ethics come in three flavors: aspirational (what would we like everyone to do?), regulatory (what must we do?) and educational (why should we do this?). Education researchers Felice Levine and Joyce Iutcovich have made a related distinction, noting that such guidelines generally focus on “(1) general education and professional development, (2) prevention and advisement and (3) complaint handling and enforcement of codes of ethics.” Levine and Iutcovich add that societies also vary in the level of effort they devote to each objective. But our committee did not begin by contemplating either set of distinctions—or how much effort we would expend. We started out developing what would have been, in retrospect, a brief set of aspirational guidelines. But over three years, we transitioned to a more regulatory and educational approach, so that our final document included extensive discussion and reasoning for each guideline. I believe that this approach made the document not only more valuable but also more honest. By forcing ourselves to justify each directive, we found instances in which we could not do so. And rather than use the “because we said so” explanation, we modified the guidelines. For some topics, our guidelines were at odds with the codes of other organizations, and we were explicit about this in our document. A case in point involves the matter of placing prepublication copies of manuscripts on a website. Although this practice is common in some fields, such as physics, some journals do not wish to consider a manuscript By forcing ourselves to justify each directive, we found instances in which we could not do so. And rather than use the “because we said so” explanation, we modified the guidelines. 30 Making Ethical Guidelines Matter that has already appeared on the Web or been circulated widely among colleagues. They may consider such papers to have been previously published or to have lost their novelty. But our committee felt that both practices were not only acceptable but desirable because they helped promote communication among scientists. We did, however, feel obliged to warn authors that, if they followed our recommendations, they might risk having certain journals refuse their manuscripts. Conundrums The question of sharing manuscripts evoked little debate in our committee or in the governing council of the SfN. Some issues were even more straightforward: One cannot imagine, for example, a serious argument in favor of falsifying data. But few aspects of responsible conduct are so simple. Like most sets of guidelines, our document dealt with many subtler issues, some of which have led to a good deal of discussion. Among them were authorship, dual publication, plagiarism and sharing reagents. Authorship: Should the head of a research group automatically be listed as an author of every publication that derives from his or her lab? Does a technician who spent many hours collecting valuable data qualify as an author? The SfN guidelines say no in both cases, stating clearly that intellectual contribution is an essential criterion for authorship. But it took a lot of discussion for our committee to reach this position, and it is still not universally accepted within our field. Dual publication: Although we encouraged informal sharing of manuscripts, our guidelines say that publishing the same material in two primary research journals is always wrong. But what if an author works in a country where English, the language of nearly all internationally known journals, is not well understood by those who would benefit from reading the paper? In such cases, a translation could be beneficial, and some have argued that the “no dual publication” rule hampers the distribution of knowledge. Plagiarism: The prohibition against publishing someone else’s text or data without permission is clear enough, but what about the use of someone else’s ideas? If, for instance, a 1993 publication by Jones states: “We believe that maternal stress often leads to a marked change in the endocrine response to stress in offspring,” then the use of those very words would require quotation marks and a specific reference to Jones, 1993. But what if a later author writes: “We think that stressing a mother can alter the hormonal reaction to a stressor in neonates”? Quotation marks are no longer appropriate, but surely the minor change in wording still warrants a reference to Jones. How many words must one change to absolve oneself of providing a citation? Often this is a judgment call, but it is always better to err on the side of giving Jones some credit. Michael J. Zigmond 31 Sharing research reagents: The SfN guidelines are quite emphatic about this, stating that “unique … materials used in studies being reported must be made available to qualified scientists for bona fide research purposes.” This directive is consistent with the regulations of most biomedical journals and funding agencies. But what of the student who spent years developing a reagent in order to conduct specific experiments and now wishes to reap the benefits? Surely, in evaluating what is best for science, one should also consider what is best for the careers of scientists, especially junior ones. This tension became all too clear to me at an event that I wrote about in 2003 in Science and Engineering Ethics. I quote from that report: How many words must one change to absolve oneself of providing a citation? A year after the publication of the [SfN] guidelines I decided to help promote an awareness of the document by organizing a workshop at a small conference of neuroscientists. My focus was on the stipulation that authors be prepared to share with other investigators any materials developed in a lab and described in a peer-reviewed publication—a requirement that … had been considerably strengthened as a result of input to the guideline committee. I invited several “opinion leaders” to help with this task, including a member of the editorial board of a prominent neuroscience journal and the director of a federal agency that supports research in neuroscience. To bring a little bit of levity to an otherwise very serious discussion, party hats were provided for each of the discussants. For example, the editor was given the shade of a copy editor and the director of the funding agency received Uncle Sam’s top hat. Then I distributed an ethics case: “Dr. Michelle Tyson is happy. She has just completed three years of hard work as a postdoc and has a great deal to show for it: She’s developed a knockout mouse (Syko) that is a model for schizophrenia, published a paper on that mouse in a prestigious journal, and has secured an assistant professorship at State University. She knows that the new mouse and the paper were critical in getting her the job and she’s ready to show the search committee that they did the right thing: She will immediately set up her new lab and then begin to reap the benefits of her hard work by exploring the neurobiology of this mouse. However, no sooner had she arrived at State University, than she received an email message from Dr. Max Megalab asking her to provide a dozen mice from her Syko colony. It is clear from the email that Dr. Megalab understands the potential of the mouse line and will have no trouble figuring out and completing the very experiments that Dr. Tyson had plans to pursue. Should Dr. Tyson provide the mouse?” Imagine my surprise when no one on the panel felt that Dr. Tyson should provide the mouse and thereby follow the guidelines for sharing! Instead, concerns were raised about the fairness of asking a hardworking junior 32 Making Ethical Guidelines Matter researcher to turn over the fruits of her labor to Dr. Megalab, the possibility that people would rather postpone publication than share a unique resource that was critical to their ongoing experiments, the absence of funds to facilitate the distribution of those materials, or the means by which the guidelines would be enforced. (For comments on this case, see [http://skillsandethics.org].) I was still trying to deal with this unexpected outcome the next morning when I returned to the location of the workshop only to discover that my own key reagents—the party hats— had apparently been stolen! I have not tried to repeat this experiment. In a recent review of the original guidelines, the SfN reaffirmed its mandate that reagents must be shared if they are not otherwise available— a practice that reduces the waste of funds for making duplicate reagents and also promotes attempts to replicate published results. But just as in the case of honorary authorship, the regulation is not universally followed. The Big Thaw If some senior scientists refuse to follow an ethical guideline even in a mere case study, perhaps it is fair to ask: Do guidelines for responsible conduct matter? Do they make a difference? Unfortunately, we have little information with which to evaluate this essential question. But then, we actually have little information about the impact of any ongoing effort to reduce scientific misconduct—behaviors that are almost certainly very rare but are nonetheless of great significance to science. And we must ask, as we do of the proverbial tree falling unheard in the forest, does a set of guidelines that remains unread make a sound? In “Honesty” (Chapter 1), John Ahearne quoted the Roman poet Juvenal, who observed that “honesty is praised and then left to freeze.” And Caelleigh has written: Anyone who works to change human behavior engages in “magical thinking” at some point—such as the irresistible hope that small, simple changes can produce large, complex results in behavior.… Magical thinking also underlies the situation when a scientific society passes a resolution that its members are committed to the highest standards in all aspects of research and then, based on the resolution alone, expects members to meet the standards. As the chair of the initial SfN committee on guidelines for communicating research findings, I worried a great deal about the fate of our document. How might we avoid letting our guidelines “freeze,” sitting in the archives only to be thawed when a potential ethical breach was discovered and procedural guidelines were required? How would we avoid “magical thinking”—something that should, after all, be anathema to any group of scientists? As a researcher in the field of brain disorders, I am interested in preventing diseases as well as treating them, and I Michael J. Zigmond 33 believe that guidelines should serve a similar pair of functions. Thus, my colleagues and I have sought ways to make our code a more effective educational tool, not just a reactive mechanism to deal with misconduct. And I believe that we are beginning to be successful. To accomplish this, the SfN has added to its lively array of lectures and workshops on ethics, providing several specific programs that complement the guidelines. This has been particularly evident since 2010, when the society issued revised guidelines for responsible communication and established an e-mail address through which individuals can make comments or raise questions about those guidelines. The SfN has also recently hosted two international symposia on responsible conduct in communicating scientific results, along with a two-day workshop on the subject. And the society has commissioned a manual that will contain its guidelines on research communication along with related ethics case studies, discussion notes and a bibliography for further reading. That manual will be ready for distribution to SfN members and other interested individuals later this year. We anticipate that it, too, will help the guidelines serve the educational purpose for which they were designed and keep them from being relegated to the archives. I urge other professional societies to take similar approaches if they have not already done so. Let us do away with magical thinking and rewrite Juvenal’s quote to state: “Honesty is praised and then helps us change the world around us!” Michael J. Zigmond is a professor of neurology, psychiatry and neurobiology at the University of Pittsburgh. He is a past secretary of the Society for Neuroscience and past president of the Association of Neuroscience Departments and Programs. 35 5 Digitizing the Coin of the Realm Electronic publication has transformed the culture of scientific communication Francis L. Macrina Imagine it’s 1991. You’ve just completed a series of exciting experiments in the lab and now it’s time to write up the results. You review the instructions for authors of the journal where you will submit your paper and you consult some rudimentary authorship guidelines published by your scientific society. You are even inspired to reread a few sections of Robert Day’s classic book How to Write and Publish a Scientific Paper, then in its third edition. (It’s now in its sixth.) Engaging your coauthors, you work diligently for a few weeks to draft and revise your manuscript. Finally, you package the printed pages, attach the correct postage, and get ready to hoof it over to the campus postal drop. Before you leave your office, you power down your desktop computer. As its cooling fan turns quiet, you never imagine that in 20 years, you’ll be able to carry orders of magnitude more computing power in your pocket. Scientific Currency Over the past two decades, computing has transformed scientific publication, a process so central to the research enterprise that it is often called the “coin of the realm.” Sociologist Robert K. Merton is credited with introducing that phrase in the context of science. As he explained in his 1968 article, “The Matthew Effect in Science,” Merton intended the “coin of the realm” to refer to recognition by one’s peers for one’s work. But over time, the phrase has become more broadly connected with the concept of authorship. Nuances aside, publishing one’s research results is a critical step in earning peer recognition. It is also essential for the progress of science. The value of publishing scientific results has always been indisputable and it will remain so. But virtually every aspect of the process is, or soon will be, affected by the digital revolution. Generally, scientists have accepted these changes, assuming or hoping they were for the better. As the digital landscape 36 Digitizing the Coin of the Realm In 1991, when it came to scientific publication, computers weren’t much more than word processors. continues to evolve, we need to think about and systematically examine the impact technology is having on the coin of the realm. This reflection should lead to engagement and action by the community of science—editors, publishers, scientific societies and scientists themselves—to ensure that the digital revolution has the maximum positive effect on the reporting of research. I hope that this essay will stimulate such thinking. That Was Then Twenty years ago, you would have used your personal computer solely as a means to prepare your manuscript. In 1991, when it came to scientific publication, computers weren’t much more than word processors. But the winds of change were already blowing, and some aspects of the electronic preparation of your 1991 manuscript did portend things to come. Computers were making it easier to create complex, high-quality illustrations. You would have used a software program to compile your list of literature cited and to insert citations into your manuscript. Such programs provided relief from the burdensome job of building reference lists, and they were harbingers of the effect digital tools would have on scientific publication over the next two decades. For historical perspective, consider the following 1991 truisms. Communication by e-mail was growing rapidly, but e-mail attachments were still a few years away. Manuscript submission and review were solidly grounded in paper and the postal service, but facsimile machines were beginning to accelerate the process. The rise of electronic journals and open-access publication was years in the future. Unless you were in the computer sciences, you probably had not heard of the World Wide Web project. Digital photography was an emergent technology, but the Adobe corporation had only recently launched version 1.0 of Photoshop. And the now-ubiquitous Adobe Portable Document Format (PDF) did not yet exist. You can expand this list yourself, but I trust I have made my point. These elements have all contributed to the rapid transformation of scientific communication. This Is Now: From Print to Pixels Let’s take a look at where things stand today by considering how computers, computing, and the Internet have affected the publication process itself. The availability of detailed, quality information about how to publish our scholarly work has grown dramatically, creating a valuable resource that is just a few mouse clicks away. The spartan instructions for Francis L. Macrina 37 authors (IFAs) of the early 1990s have given way to complex web pages and downloadable electronic files. Along the way, IFAs themselves have changed from brief documents that conveyed preparative and administrative instructions to lengthy, detailed compendia of authorship definitions, responsibilities, expectations and policies. In 1991, the IFA for the journal Nature amounted to a single printed page of 1,300 words. Today, Nature publishes its IFA electronically as the “Guide to Publication Policies of the Nature Journals.” It is an 18-page, 12,000-word PDF. Such evolution is more likely to be the rule than the exception. I recently reviewed the publication guidelines of five scientific journals for a study that appeared this year in Science and Engineering Ethics. Most of these journals had expanded their IFAs into detailed documents. I also looked at guidelines provided by a few professional societies and noted that they, too, contained considerable detail about authorship and publication practices, much of which agreed with the journals’ IFAs. In “Making Ethical Guidelines Matter” (Chapter 4), Michael Zigmond made a compelling case for the role that professional societies can and do play in developing and promoting codes of conduct. Zigmond chaired the Society for Neuroscience committee that wrote guidelines for responsible scientific communication. This document is so comprehensive that it leaves almost nothing to the imagination. IFAs and society guidelines have expanded for a variety of reasons. They have become more detailed and precise in response to lessons learned from high-profile misconduct cases. And they have grown longer to encompass new policies on topics such as digital image manipulation. Taken together, modern journal IFAs and professional-society guidelines form the basis for ethical standards and best practices in scientific publication. Today, this trove of information is instantly accessible using whatever electronic portal—PC, laptop, tablet or smart phone—suits you. The digital availability of information should be a Illustration by Tom Dunne. 38 Digitizing the Coin of the Realm catalyst for promoting responsible conduct, but its mere existence won’t guarantee the production of ethical researchers. We’ve got to practice what we preach, and teach what we practice. The legendary football quarterback Johnny Unitas summed it up before every game, after the coaches finished their pep talks. Unitas’s speech was always the same: “Talk is cheap. Let’s play!” Computers have not only increased the availability of ethical guidance, they have also impacted the work flow of manuscript preparation, submission, peer review, revision and publication. At one end of the spectrum, your favorite journal may have gone digital by mandating that some or all manuscript-related activities be conducted by e-mail. At the other extreme, the publisher may require the use of a web-based, graphic interface to handle all phases of submission and review, with e-mail communication augmenting the process. But across this spectrum of modern digital work flows, the common denominator is a greatly reduced role for the nonelectronic exchange of materials. Clearly, digitization makes the manuscript production-to-publication cycle more convenient for all parties, especially authors. You’ll have to accept this as my assertion based on experience and intuition, because data to support the claim are scarce. But if you published papers 20 years ago, and still do so today, you’ll know what I mean. I believe that most scientists do not miss drawing figures (even with early computer programs), photocopying manuscripts and mailing printed papers. But the notion of convenience should not be confused with speed. To be sure, the time between acceptance and publication has gotten shorter: just a few weeks for online articles, compared to months for print articles. But there’s also the issue of the time from submission to acceptance. If you look at papers published online, you’ll likely find that the time between submission and acceptance can be a few months, sometimes longer. The obvious interpretation is that peer review can take varied, unpredictable and sometimes excessive amounts of time. This may reflect a process that is desirably rigorous. But excessive submission-to-acceptance time can also be a sign of the human foibles of overcommitment or procrastination. Evidently, even the most attractive graphic interface can’t overcome these age-old problems among authors, editors and reviewers. The digital availability of information should be a catalyst for promoting responsible conduct. Instant Feedback The online revolution has changed the way papers are read and evaluated after they’re published. Studies were once critiqued in formal letters and reviews—often published in the same journals as the Francis L. Macrina 39 original papers—and in journal clubs and discussions. The visibility and pace of those critiques have exploded with the advent of blogs and other online venues. For example, an initiative called Faculty of 1000 was established in the early 2000s as a corporate endeavor to provide postpublication peer review online. The program selects and enlists scientists, termed faculty, to scan the literature and comment each month on the papers they consider most interesting. Their reviews, which highlight good articles and provide constructive criticism, are available by subscription. Subscribers may also log in and comment on any evaluated article, but the site is systematically monitored for inappropriate commentary. Abusive, defamatory or otherwise offensive remarks can be reported and may be deleted by the service provider. Such consistent controls are not necessarily in place on independent blogs, which have also taken on an increasingly visible role in postpublication peer review. One notable example began to unfold in 2010, when Science magazine published online a research paper about a bacterium isolated from arsenic-rich lake sediments. The authors reported that this organism could incorporate arsenic, instead of the usual phosphorus, into its DNA. The biological implications of the work were huge, and the paper got considerable exposure in the media. It also attracted scrutiny from scientists who used their blogs to offer a variety of critical comments. But these evaluations were met with disdain by the paper’s authors, who said they would only respond to critiques that had been peer reviewed and vetted by Science. Rather than engage with their critics, the authors simply asked scientists to work to reproduce the controversial results. This attitude prompted the journal Nature to publish an editorial which asserted that there is indeed a role for blogging in the assessment of published results. Still, for some scientists, the speed and directness of unvetted digital criticism popped up unexpectedly. A subsequent news article in Nature, cleverly titled “Trial by Twitter,” claimed that “blogs and tweets are ripping papers apart within days of publication, leaving researchers unsure how to react.” That may be so. But fast-forward a few months for a completely different take on the social networking of scientific data. One of the largest outbreaks of potentially lethal Escherichia coli infections began in Germany in May 2011. In about six weeks, there were more than 3,000 cases and 36 deaths. Scientists on multiple continents shared biological samples and used online media such as Twitter, wikis and blogs to compile their data. Within 10 days of the recognition of the outbreak, the entire genomic sequence of one of the isolated E. coli strains was available on the Internet. As I write, data analysis is still underway, but the collaborative research has already yielded new and valuable information about the E. coli strains involved. The speed and real-time availability of this genetic analysis is unprecedented and underscores 40 Digitizing the Coin of the Realm Electronic publication has transformed scientific communication over the past 20 years. A process that was once grounded in paper and the postal service (left) is now conducted almost entirely online (right). The changes have been most profound for open-access journals (center), which provide free access for readers. Although many subscription-based publications (far right) continue to print their journals, electronic publication has accelerated the exchange of information. (Illustration by Barbara Aulicino.) Francis L. Macrina 41 a powerful use of digital social media in the dissemination of new scientific knowledge. Access for All Earlier in this essay, I discussed online publication of articles as a service provided by publishers to complement the printed versions of their journals. This form of electronic publication still requires users to have a subscription or an institutional site license to access online articles. But a second, slower-growing form of publishing, which also began in the 1990s, lets readers access online articles for free. The business model for such publications depends on the relatively low cost of distributing digitally encoded articles. And the expenses of doing so are borne by the authors themselves or by their academic institutions or funding agencies. At a meeting in 2003, a group of scientists, librarians and publishers wrote a document now commonly known as the “Bethesda Statement on Open Access Publishing,” which has been widely embraced among open-access (OA) publishers. The statement lays out two conditions that define OA publication. First, it grants “to all users a free, irrevocable, worldwide, perpetual right of access” to the published work, as well as a license to “copy, use, distribute, transmit and display the work publicly,” to distribute derivative works based on the original and to make a few copies for personal use. Second, it promises that the work will be deposited in at least one online repository that is supported by an academic institution or other “well-established organization” that supports open access and long-term archiving. In practice, this definition has been widely adopted, with individual variations among publishers. Although it had a slower start than subscription-based online publishing, the OA model is now viable and growing. A website called The Directory of Open Access Journals reported the existence of 6,671 OA journals in all scholarly fields at the end of June 2011. And in a study published this year in the OA journal PLoS ONE, Mikael Laakso and colleagues reviewed 16 years of OA publishing, from 1993 to 2009. They report that the number of such journals grew 18 percent per year, while the total number of scholarly journals grew only 3.5 percent per year. The numbers of OA journals and articles show impressive growth curves over the time frame. But despite the increase, these articles accounted for only about 8 percent of all scholarly papers published in 2009. Other studies have shown that researchers are well aware of OA journals and increasingly publish their work in them. Perceived advantages include free accessibility to users and the ability to reach a wide readership. The validity of criticisms, such as diminished prestige and lower peer-review quality, remains unresolved. The acceptance of OA 42 Digitizing the Coin of the Realm publishing and the success of the enterprise may be best expressed by the fact that PLoS ONE published 6,749 papers in 2010, making it the world’s largest journal that year. Today, free access is part of the culture of scientific publication. But it will be interesting to follow the trends as new publishers enter the marketplace and authors develop a better sense of the desirability (or undesirability) of publishing in OA journals. OA publication is often referred to as an “author pays” model, in contrast to the alternative, in which the user pays a fee to gain access. Typically, authors have always paid to publish their work. In 1991, authors often spent several hundred dollars on page charges and reprint fees for a single paper. But for OA publication, the author pays even more. These journals charge an article-processing fee that can range from about $1,000 to several thousand dollars, depending on the journal. If you publish in a subscription-based journal that distributes articles in print and online, and also offers an OA option, you rack up additional fees. Today, page charges are $50 to $100 per page, which would get you into print and online and make your paper accessible to journal subscribers. Then, you might want to publish supplemental information on the journal’s website, for a surcharge of up to several hundred dollars. Finally, you might decide to make your article freely available from the moment it appears online, a decision that may cost you several hundred to thousands of dollars more. Today, as in the past, most journals waive or reduce page charges or OA fees if the author demonstrates that he or she cannot afford them. Although OA journal publishing is the dominant means for putting scientific results into the public domain, other strategies do exist— and all are facilitated by online technology. Journal articles may be deposited into any of several public-domain digital archives such as PubMedCentral. Subscription-based journals may allow authors to pay an extra fee to make their papers freely available online. Finally, researchers may post OA manuscripts on noncommercial servers such as arXiv.org, or on personal or institutional websites. Pondering the Power of Pixels For more than 20 years, we have witnessed the profound effects of digital technology on scholarly publication. Changes in logistics and culture have been diverse and numerous. But I would argue that today, open access is the central issue in the marriage of publication to the pixel. It may be growing too fast for some and not fast enough for others, but it is growing nonetheless. I believe it is here to stay. It takes multiple forms, from journals that exclusively practice free-to-user availability, to individual investigators who maintain online libraries of their own published work. Will one model dominate over time? Are there more models to come? If the past 20 years are any predictor, the Francis L. Macrina 43 interplay of imagination, market forces and evolving digital technology will continue to change the publication landscape. In the meantime, the scholarly community has a role to play in the development of the OA movement. That community includes authors, publishers, scientific societies, librarians and computer scientists. OA journal publishing should be subjected to ongoing evaluation to measure its impact, to address problems and to improve the platform for all its users. There should be transparent assessment of performance metrics such as article processing times, citations, peer-review quality and the costs to those involved. Once such evaluations have been performed, they may help answer a growing host of questions: Is a goal of 100-percent open access reasonable or desirable? Should researchers embrace some forms of OA publication and not others? What about server space, backup and security issues specific to online-only journals? As we move toward a more OA culture, what role do—and should—printed journals have? Should there be more proactive education about OA publication? Do we need to be more forward thinking about who should pay for publication costs? Many research-funding agencies do pay grantees’ publication fees, but with OA publishing, the budget may have to increase. Should our institutions step up to the plate with their checkbooks? To gain maximum effect, the analyses that address these questions should be made by parties devoid of conflict of interest, and—in the spirit of open access—the results should be placed in the public domain. Francis L. Macrina is the Edward Myers Professor of Dentistry and Vice President for Research at Virginia Commonwealth University. He is past editor-in-chief of Plasmid and has served on the editorial boards of the Journal of Bacteriology; Infection and Immunity; and Antimicrobial Agents and Chemotherapy. He has served on the ethics practices committees of the American Society for Microbiology and the American Association for Dental Research. Acknowledgments I thank Andrekia Branch for her help in manuscript preparation and Glen Kellogg for helpful comments. 45 6 Raising Scientific Experts Competing interests threaten the scientific record, but courage and sound judgment can help Nancy L. Jones I would be a wealthy woman if I had a dollar for each time a student, a postdoctoral fellow, one of my colleagues—or even I—moaned and groaned about the capriciousness of scientific peer review. Some newbies are stymied in front of their computer keyboards for months as they write their first manuscript, trying to organize their meandering paths of research and messy, gray data into logical experimental designs and strong conclusions. Others, demoralized by pithy, anonymous critiques (surely from their toughest competitors), have to muster all their restraint to keep from writing scathing, retaliatory responses to their reviewers. I remember my own qualms on one of the first occasions that I evaluated grant proposals with a panel of reviewers. I felt certain that my lack of gamesmanship was the reason a few outstanding applications were not funded. While I reviewed my assignments using the criteria given, other reviewers adamantly championed—and got more attention for—the best of the proposals they evaluated. No one had prepped me for how the review committee would operate. Peer review is one of the central activities of science, but students and trainees are often ill prepared to assume their duties as authors and reviewers. Clearly, there is more to peer review and publication than factual knowledge and technical skills. Science is a culture. To succeed, we need to nimbly navigate within our professional culture. There is much that training programs can do to instill professionalism in the next generation of scientists, and I will outline some of the approaches that my colleagues and I used to develop an ethics and professionalism curriculum at Wake Forest University School of Medicine (WFUSM). But first, if we are to aspire to excellence in scientific publication—and train young scientists to do the same—it is important to understand the purpose of scientific publishing and the competing interests that may compromise it. 46 Raising Scientific Experts Research findings must be reported in an accurate and accessible way that allows other scientists to draw their own conclusions. The Ideal The central role of publication is to create a record that advances collective knowledge. When research and scholarship are published in a peerreviewed journal, it means that the scientific community has judged them to be worthwhile contributions to the collective knowledge. That is not to say a publication represents objective truth: All observations are made in the context of the observer’s own theories and perceptions. Research findings must, therefore, be reported in an accurate and accessible way that allows other scientists to draw their own conclusions. Readers should be able to reinterpret the work in light of new knowledge and to repeat experiments themselves, rather than rely solely on the authors’ interpretations. The nature of scientific progress also requires that the scientific record include negative results and repetitions of previous studies. Reporting both positive and negative results informs future work, prevents others from retracing wrong avenues and demonstrates good stewardship of limited resources. Out of respect for the contributions of research subjects, especially humans and other primates, some argue that there is a moral imperative to publish negative results. Doing so can prevent unnecessary repetition of experiments. On the other hand, reproducibility itself is a cornerstone of science. There must be a place to report follow-up studies that confirm or refute previous findings. Finally, scientific discourse should embrace the principle of questioning certitude—reevaluating the resident authoritative views and dogmas in order to advance science. The scientific record should challenge the current entrenched ideas within a field by including contributions from new investigators and other disciplines. Examining novel ideas and allowing them to flourish helps the scientific community uncover assumptions, biases and flaws in its current understanding. In an ideal world, peer review is the fulcrum that ensures the veracity of each research report before it enters the scientific record. The prima facie principle for the practice of science is objectivity, but we all know that true objectivity is impossible. Therefore, science relies on evaluation by subject-matter experts—peer reviewers—who assess the work of other researchers. They critique the experimental design, models and methods, and judge whether the results truly justify the conclusions. Reviewers also evaluate the significance of each piece of research for advancing scientific knowledge. This neutral critique improves the objectivity of the published record and assures that each study meets the standards of its field. Nancy L. Jones 47 Illustration by Tom Dunne. For peer review to serve its intended function, authors, reviewers, editors and scientific societies must uphold certain ethical obligations, detailed in the figure on page 49. In short, authors must do their best to conduct sound, worthwhile research and openly share the results. Reviewers must be open about potential conflicts of interest, and they must provide critiques that are fair, thorough and timely. And scientific societies, as guardians and gatekeepers of their specific spheres of knowledge, must provide a normative process that ensures the rigor and validity of published results. The Reality In fact, the scientific record serves other purposes besides advancing collective knowledge. As a result, highly charged ethical conundrums emerge throughout the publication process. Science is an interactive process conducted by humans who have their own aspirations and ambitions, which give rise to competing interests—some of which are listed in the figure on page 49. The inescapable conflict in science is each individual’s underlying self-interest and commitment to promoting his or her own ideas. Furthermore, authorship is the primary currency for professional standing. It is necessary for credence and promotion within one’s home institution and the scientific community, and is essential to securing research funds. Indeed, the requirement that scientists obtain grants to support their research and salaries, coupled with funders’ accountability to the public for its investment in science, puts intense strain on the system. Increasingly, the publication record is used to weigh whether public funding for science is worthwhile. U.S. investment in science and technology has long been tied to the idea that science will give our society progress and improve our prosperity, health and security. That perspective was famously articulated in 1945 by Vannevar Bush, who was 48 Raising Scientific Experts then director of the U.S. Office of Scientific Research and Development, and it continues to shape funding for science today. Although public investment in research has sped the progress of science, it has also placed scientific communities in an advocacy role. They are no longer just the guardians of knowledge; they compete for public resources and champion their specific fields. Their advocacy cases are often based heavily on promoting the potential outcomes of research—such as cures, solutions and new economic streams—rather than justifying support for the research itself. The scientific record is not immune to this pressure. Scientific societies that publish journals can be tempted to boost the prestige of their fields by prioritizing highly speculative, sexy articles and by egregiously overpromoting the potential impact of the research. Such overpromising is particularly problematic because of the pervasiveness in our society of scientism and scientific optimism, which hold that scientific knowledge is truth. According to the philosophy of scientism, science is universal and above any cultural differences. It is immune to influences from an investigator’s psychological and social milieu or gender, and even to the scientific community’s own assumptions and politics. Under the influence of scientism, the public, media and policy makers can be tempted to apply research results without exercising the judgment needed to put them in context. Individuals who are deeply vested in scientific optimism can have difficulty seeing any potential harm as science “moves us toward utopia.” They may even become confused about science’s ability to make metaphysical claims about what life means. But the epistemology of science (how science knows what it knows) cannot support these unreasonably optimistic conclusions. Scientific knowledge is tentative. It forms through an ongoing process of consensus making as the scientific community draws upon empirical evidence as well as its own assumptions and values. And scientific models—classification schemes, hypotheses, theories and laws—are conceptual inventions that can only represent our current best understanding of reality. Although these models are essential tools in science, we must continually remind ourselves, our students and the public that conceptual models are not reality. Nor is a research article—even a peer-reviewed publication—the truth. Authors, reviewers and editors must take care to accurately communicate the kind of scientific knowledge addressed in any given publication, as well as its limitations. Authors should pay careful attention to inherent biases in their work and tone down overly optimistic conclusions. Reviewers and editors must correct any remaining inflation of the interpretations and conclusions. And scientific societies need to provide an adequate understanding of the process of science. They must convey levelheaded expectations about the speculative nature of any individual Nancy L. Jones For scientific publication to serve its intended function—to accurately advance scientific knowledge— authors, editors, reviewers and scientific societies need to meet certain obligations (top). To do so, they must also learn to manage numerous competing interests (bottom). (Illustration by Tom Dunne.) 49 50 Raising Scientific Experts study and about the time and resources that will be needed to realize the public’s investment in a field of research. Otherwise, the continued projection of scientism—science is always progress—will erode trust in science at a much more fundamental level than will the few flaws and misconduct cases that surface in the scientific record itself. Teaching Professionalism More than ever before, acquiring technical skills does not assure success as a scientist. Survival depends on operating with finesse, using what are often called soft skills. Of course scientific communities have an obligation to train their future scientists in the conceptual and methodological tools for conducting research. But they must also train students to function within the scientific culture, based on a thorough understanding of the norms, standards and best practices in the student’s specific discipline. At WFUSM, several of my colleagues and I pioneered a curriculum to promote professionalism and social responsibility within science. Our goal was to equip our students with the tools to navigate the challenging research culture with high integrity. These included soft skills such as the ability to recognize ethical issues within the practice of science, solve problems, work in groups, articulate and defend one’s professional judgment and critique the judgment of one’s peers. We also wanted to develop within each student an identity as a scientific professional, acculturated to the standards of the discipline through open communication with peers and role models. To work toward these goals, we chose a problem-based learning format, to which my colleagues later added some didactic lectures. Problem-based learning is structured around authentic, engaging case studies and requires that students gain new knowledge to solve problems in the cases. After a scenario is introduced in one class session, students seek out relevant information on their own, then apply that knowledge to the case during the next class session. Students work actively in groups, with guidance from facilitators (faculty and postdoctoral fellows) who serve as cognitive coaches rather than content experts. In our curriculum, the scenarios were designed to provide a realistic understanding of the practice of science and to prompt discussion of the norms and best practices within the profession. They also required students to identify ways that the various stakeholders—principal investigators, postdoctoral fellows, graduate students, technicians, peer reviewers and others—could manage their competing interests. We constructed activities and discussion questions so that different cases stressed distinct types of moral reflection. For example, we introduced two moral-reasoning tools, each one a set of questions that students could use to systematically sift through the principles, values and consequences in the cases. (Questions included, for instance, “What are Nancy L. Jones 51 the issues or points in conflict?” and “Can I explain openly to the public, my superiors or my peers my reasons for acting as I propose?”) Some sessions focused on moral character and competence by requiring students to solve problems and defend their decisions. Others called for students to take the perspective of a professional scientist, thereby building a sense of moral motivation and commitment. Finally, some cases cultivated moral sensitivity by presenting the perspectives of multiple stakeholders and promoting awareness of legal, institutional and societal concerns. Facilitators gave students feedback on their reasoning, moral reflection, group skills and ability to analyze problems. During a debriefing activity at the end of each case, students identified which concrete learning objectives they had accomplished. They also discussed how they were functioning as a group and what they could do to improve their team dynamic. The curriculum addressed a range of issues in ethics and professionalism, among which peer review and authorship were important themes. Cases on scientific authorship required students to investigate, between class meetings, the criteria by which their own laboratory groups, departments, institution, and professional networks assigned authorship credit. Back in class, each small group collectively assembled a standard operating procedure for assigning credit, and applied it to resolve the authorship problem in the scenario. Cases on peer review called attention to the various roles of the author, the reviewer and the editor in evaluating a manuscript. Students identified essential elements of a well-done review, the greatest ethical risks for a reviewer and strategies to mitigate those risks. Students then applied this information in their discussions of a case study in which an up-and-coming researcher was asked to review grant proposals that could influence her own research or affect a friend’s career. To refine one’s judgment requires extensive practice, a supportive climate and constructive feedback. Transforming the Culture Although my colleagues and I are confident that students benefited from our curriculum, it takes more than a professionalism course to really nurture a scientific expert. Opportunities to improve and test one’s understanding of scientific culture and epistemology should be pervasive throughout the training experience. To refine one’s judgment requires extensive practice, a supportive climate and constructive feedback. This means that mentors, graduate programs, societies and funders must value time away from producing data. Fortunately, scientific knowledge is not the data; it is how we use the data to form and refine conceptual models of how the world works. So activities that 52 Raising Scientific Experts improve scientific reasoning and judgment are worth the investment of time. More attention must be paid to the epistemology of science and the underlying assumptions of the tools of the trade. As methods and experimental approaches become entrenched in a field, rarely do students return to the rich debates that established the current methodology. This lack of understanding comes to light when prepackaged test kits, fancy electronic dashboard controls and computer-generated data tables fail to deliver the expected results. To interpret their own research and critique that of their peers, scientists need to understand the basis of the key conceptual models in their discipline. The best way to develop sound scientific judgment is to engage with the scientific community—friend and foe alike—to articulate, explain and defend one’s positions and to be challenged by one’s peers. This learning process can take place in laboratory discussions, journal clubs, department seminars and courses, as well as during professionalsociety functions and peer-review activities. As my colleagues and I learned from the evaluations of our problem-based learning course, students (and faculty) need explicit instruction on the goals, expectations and skills of these nondidactic activities. After a laboratory discussion, for example, time could be spent reviewing what was learned, giving feedback on how to develop soft skills, and providing an opportunity to collectively improve the group process. Students should be evaluated on their meaningful participation in these community activities. Professional societies also have an important role to play in fostering professionalism among young scientists. As Michael Zigmond argued in “Making Ethical Guidelines Matter” (Chapter 4), societies are uniquely positioned to develop effective, discipline-specific codes of conduct to guide the standards of their professions. Criteria and practical guides to authorship and peer review are important—but they’re not enough. We must open the veil and show how seasoned reviewers apply those criteria. Discussions among reviewers and editors about how they put the guidelines into practice are the best way to move forward ethically. Indeed, such rich exchanges should be modeled in front of the entire research community, especially for students, showing how different individuals apply the criteria to critique a paper or proposal and then respectfully challenge each other’s conclusions. Societies and funders could also provide sample reviews with commentary on their strengths and weaknesses, and how they would be used to make decisions about publication or funding. As graduate programs and societies implement such programs, they also need to ask themselves if their activities are actually conducive Criteria and practical guides to authorship and peer review are important— but they’re not enough. Nancy L. Jones 53 to open scientific dialogue. Sometimes, the cultural climate stifles true engagement by tolerating uncollegial exchange or by allowing participants to float in unprepared for substantive discussion. There must be a spirit of collective learning that allows students to examine the assumptions and conceptual models that are under the surface of every method and technique. No question should be too elementary. Arrogant, denigrating attitudes should not be tolerated. Finally, scientists should foster commitment to their profession and its aspirations and norms. This goal is best accomplished through frank discussions about how science really works and about the various competing interests that pull on a scientist’s obligations as author, peer reviewer and, sometimes, editor. Many students enter the community vested in scientism—living above the ice-cream parlor, if you will. Viewing life through those idealistic, optimistic lenses causes them to stumble into an epistemological nightmare the first time they try to make black-and-white truth out of their confusing data. Or even worse, they become sorely pessimistic after naively smacking headfirst into the wall of disillusionment when trying to publish in a prestigious journal or competing, for the first time, for an independent research grant. We must provide opportunities that afford socialization around the principles, virtues and obligations of science. Our faculty and trainees should freely discuss how they have dealt with their own competing interests and managed conflicts within peer review and authorship. All participants need to enter these conversations with a willingness to learn from others and address how to improve the culture. I’ll end by positing a new definition of professionalism: A scientist, in the face of intense competing interests, aspires to apply the principles of his or her discipline to support the higher goal of science—to ethically advance knowledge for the good of humankind. Professionalism takes courage, but when leaders display this courage, the journey for those who follow is better. Nancy L. Jones is a health-science policy analyst at the National Institute of Allergy and Infectious Diseases. She received a Ph.D. in biochemistry from the Wake Forest University School of Medicine (WFUSM) and an M.S. in bioethics from Trinity International University (TIU) in Deerfield, Illinois. 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