J Neurol DOI 10.1007/s00415-015-7858-5 ELECTRONIC SUPPLEMENTARY MATERIAL And Pavlov still rings a bell: summarising the evidence for the use of a bell in Pavlov’s iconic experiments on classical conditioning S. Jarius1 • B. Wildemann1 Received: 2 July 2015 / Revised: 9 July 2015 / Accepted: 12 July 2015 Abstract The iconic ‘dog-and-bell scenario’ used to illustrate the concept of classic conditioning developed by the Russian physiologist Ivan Petrovich Pavlov (1849–1936) in most textbooks in the field of neurophysiology and psychology has been repeatedly put into question. Here, we summarise and critically discuss the available evidence for and against the occasional use of a bell in Pavlov’s laboratory from his own writings and those of his co-workers and, in addition, re-present new pictorial evidence. We conclude that the ‘dog-and-bell scenario’ indeed has a factual basis, but is strongly influenced by a verifiably incorrect 1928 report in the then widely read Time magazine. Keywords Ivan Petrovich Pavlov; classical conditioning; unconditioned stimulus; bell. The term ‘classical conditioning’ (CC) is used to refer to a process of learning that is induced by the repeated pairing of a neutral stimulus (NS) with a potent biological stimulus (so-called unconditional stimulus), eliciting a usually innate reaction (the so-called unconditional response, UR). CC results in the NS becoming a more or less potent, socalled conditional stimulus able to elicit the UR (which then is called a conditional response, CR). Although the concept as developed by Pavlov has been repeatedly challenged, it has become the foundation of the modern science S. Jarius, [email protected] 1 Molecular Neuroimmunology Group, Department of Neurology, University of Heidelberg, Otto Meyerhof Center, Im Neuenheimer Feld 350, 69120 Heidelberg, Germany of learning and, in particular, of the influential theories of Watson and Skinner and the entire school of behaviourism. In a recent article on the life and achievements of the Russian physiologist Ivan Petrovich Pavlov (1849–1936) in the January 2015 issue of this journal [8], the authors questioned whether Pavlov ever used a bell in his experiments on CC: “Nowadays, we reflexively link his name to a dinging bell and a drooling dog, although he never trained a dog to salivate to the sound of a bell [8]. Our brains have been conditioned with [a] myth” [8]. This is in line with at least three previous authors who stated they “hunted in vain for any such mention” [7] or “have not yet found any experiment in which a bell was used” in Pavlov’s works [9, 16]. However, this notion has been refuted by others and characterised as “the myth of a myth” [26]. To shed some more light on this issue we decided to investigate the evidence in favour of Pavlov’s use of a bell in more detail. Given that the ‘dog-and-bell scenario’ is described in almost all major textbooks and has become ‘common knowledge’, this seems to be a matter of more general interest. To clarify the issue further, we first screened all of Pavlov’s works included in the two volumes of the 1941 edition of Lectures on Conditioned Reflexes (Volume 1: Twenty-five years of objective study of the higher nervous activity (behaviour) of animals; volume 2: Conditioned reflexes and psychiatry) [21], which contains a compilation of Pavlov’s speeches and articles. Both volumes were translated and edited by W. Horsley Gantt, a pioneer in psychophysiology, whose work is reflected in seven books and more than 700 publications [14]. Gantt was a coworker of Pavlov from 1925 to 1929 and later director of the Pavlovian Laboratory at Johns Hopkins University as well as initiator and long-standing editor of the Conditional J Neurol DOI 10.1007/s00415-015-7858-5 ELECTRONIC SUPPLEMENTARY MATERIAL Reflex Journal (published under the auspices of the Pavlovian Society); he can thus be considered a credible source. Of note, his 1941 edition also contains Pavlov’s later writings, published between 1928 and his death in 1936. By contrast, previous authors interested in the “dogand-bell” riddle [7, 9, 16, 26] mainly used Gleb Vassilievitch von Anrep’s (1891-1955) [10] 1927 edition of Conditioned reflexes. An investigation of the physiological activity of the cerebral cortex [17] – a different book from that translated by Gantt despite the similar title. In Gantt’s edition of Pavlov’s works, we found numerous mentions of a “bell”. In Destruction of the skin analyser (read before the Society of Russian Physicians and published in Transactions of the Society of Russian Physicians, 1910–1911) Pavlov reports a series of experiments based on observations by N. M. Saturnov from his laboratory. He gives a very clear description of the typical CC experiment to which most modern textbooks refer: “You see that the dog is now quiet, and that saliva does not flow spontaneously. The bell begins to ring. The dog moves and looks for food, and 9 drops of saliva appear – clearly a normal reaction. The bell is obviously a conditioned stimulus. This demonstration is so evident that it is not necessary to show you other sound reflexes.” (vol. I, p. 166) A bell is also mentioned in Scientific study of the socalled psychical processes in the higher animals (vol. I, p. 89), in Internal inhibition and sleep – one and the same process (vol. I, p. 312), and in The inhibitory type of nervous systems in the dog (vol. I, p. 364-365, “the former strongest of all the conditioned stimuli, viz., the bell”), where we read: “All the auditory reflexes were one and a half times or twice as great as the optical. The bell occupied first place among the sounds, next came the metronome, and the weakest of all was the whistle.” (p. 364). In A physiological study of the types of nervous systems, i.e., of temperaments (p. 372), Pavlov states: “If you whistle, or ring a bell, or raise the hand, or scratch the dog – whatever you will – and now give the dog food and repeat this several times, then each one of these stimuli will evoke the same food reaction: the animal will strive toward the stimulus, lick his lips, secrete saliva, etc., – there will be the same reflex as before”. Of note, Pavlov still mentioned a bell (besides a rattle) in some of his latest works (cf. vol. II, chapters XLVII and LVII of the 1941 edition of Gantt’s English translation). A bell is also explicitly mentioned in Gantt’s introduction to his translation of Pavlov’s Lectures: “The intensity of the conditioned reflex has been shown (…) by Pavlov (…) to depend also upon the intensity of the conditioned stimulus – a loud bell produces a greater food excitation than a faint one (…) within certain ranges” (p. 13 of the 1941 edition). Here, Gantt possibly referred to a work by Kupalov, Lyman and Lukov from Pavlov’s laboratory published in 1931 in Brain [15] that indeed made use of a bell. Finally, Pavlov’s refers to a bell also in his famous Huxley lecture read at Charing Cross in 1906, which was published in The Lancet [19] (and, and in a condensed form, in the British Medical Journal [20]). However, the lecture was “[s]pecially translated for The Lancet” and the original version is, to the best of our knowledge, lost†. While the wording of Gantt’s version of that lecture is different from that published in The Lancet [19], both translations consistently use the phrase “ringing of a bell” when speaking about acoustic stimuli. However, it is not completely clear what types of bells were used. In his 1927 translation of the third lecture in Pavlov’s Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex (1927; Dover, New York), in which an experiment illustrating the development of a secondary conditioned reflex is described (Lecture III), Anrep mentions an ‘electric bell’‡: “A dog has two primary alimentary conditioned stimuli firmly established, one to the sound of a metronome and the other to the buzzing of an electric bell.” (p. 34) Going back to the Russian original text [27], we found that where Anrep writes, “the buzzing of an electric bell”, Pavlov simply used the single word “звонок”. The same word, in other instances, was translated as “bell” by Gantt. By contrast, in Lecture VIII, in which Pavlov speaks about compound stimuli, Anrep confusingly uses the word “bell”, too, where Pavlov has “звонок”: “In other experiments the stimulatory compound was made up of three or four different stimuli all belonging to one analyser; the stimuli were made to succeed one another in a definite order, being each of equal duration, and with equal pauses between them. There were used, for example, in one case the four tones C, D, E, F of one octave; and in another case the four stimuli were made up of a noise, two different tones and the sound of a bell.” Did Anrep have more detailed knowledge of the setup of those experiments that allowed him to make such specific distinctions? It seems highly unlikely that specific † According to a report in Science [18] and as suggested by the many German terms given in parenthesis in the English translation [19], the speech was originally delivered by Pavlov in the German language. ‡ Electric bells were invented in the 1830s [13] and had become commonplace by the early 1900s. J Neurol DOI 10.1007/s00415-015-7858-5 ELECTRONIC SUPPLEMENTARY MATERIAL changes to the text such as those in lecture III were not made deliberately: Like Gantt, he had been a close collaborator of Pavlov in the past and worked with auditory stimuli himself [5]§. Moreover, (in the foreword to his edition) he emphasised that all changes he introduced to the original text were made with the agreement of Pavlov**. However, it is also possible that this inconsistency reflects editorial negligence. First, Anrep, who was not a native English speaker, employed (as he states in the same foreword) professional translators funded by the Royal Society to generate a draft translation of lectures I-XII, which he then finalized. Second, he had to work under substantial time-pressure from the time he learned about Gantt’s independent translation of Pavlov’s Twenty years of objective study (appealing to Pavlov, Anrep could stipulate only a six months delay in publication of Gantt’s book [25]). On the other hand, Gantt was both a native English speaker and had worked at Pavlov’s laboratory in Leningrad for altogether six years. Why would he not employ the word buzzer, electric bell, or doorbell in his translations whenever such a device had been used? In 1976, Gantt should still use the term “bell”. In that interview (see [14] for a complete transcript), Gantt declares that he employed a “bell [as] the signal for food” in his own laboratory at the Johns Hopkins University and emphasises that he employed “the same methods” in his dog experiments “as [he] had learned from Pavlov”. Beside Gantt’s, there is a second personal testimony: Tully (2003) refers to Petr Kuzmich Anokhin (1898–1974), the father of the ‘feedback’ concept and one of the founders of the Institute of Psychology of the USSR and the Laboratory of Neurophysiology of Training, as a witness. According to Tully, Anokhin had “documented” the use of “two bells” in Pavlov’s experiments, a “звонок” and a “колоко́льчик" (the latter of those two words more transporting the idea of a traditional [hand]bell) [26]. In their abovementioned study, Kupalov and his colleagues concluded that “noises or more impure tones” (air bubbling through water and, explicitly, a “bell” are given as examples) produce stronger and more consistent conditioned reflexes than “pure (sine wave)” stimuli and specu- lated that the auditory cortex of mammals may not be made “for the hearing of tones but for the hearing of noises”, suggesting that a non-electric bell may possibly have been employed [15]. Kupalov’s findings, by the way, seem to qualify, at least to some extent, the stance expressed in Todes’ splendid recent book on Pavlov’s life, which has it that the use of a bell would have been contra-intuitive since Pavlov’s experiments required “precise control” of the quality of the stimulus [25]. As the contemporary meaning of “звонок" (sometimes we read “обычный [i.e. conventional] звонок” [15]) is not unequivocal and as we could not find any account of the word “колоко́льчик" in Pavlov’s writings, we set out to look for pictorial evidence. First, we screened a large number of original publications from Pavlov’s group for figures depicting the experimental setting. While this search was mostly unrevealing, we found an highly interesting image in Pavlov’s ‘official’ biography, published in 1953 by the Academy of Science of the Soviet Union and authored by Pavlov’s pupil Ezras Asratovich Asratyan (1903–1981), then head of the Institute of Higher Nervous Activity and Neurophysiology founded after the infamous ‘Pavlovian session’. This drawing of the dog chamber in Pavlov’s laboratory (Fig. 1) depicts a conventional bell (besides metronomes and a light bulb, two other frequently employed stimuli) fixed to the wall [6]. We are not aware of any previous publication on the issue in question noting this image. Second, we would like to draw attention to the 1926 Soviet educational film Mechanics of the Brain (original Russian title Механика головного мозга), directed by Vsevolod Illarionovich Pudovkin (1893-1953), an early attempt to popularise Pavlov's studies in classical conditioning that was formerly accessible only at a few film institutes worldwide [24] but is now available as an internet resource [23]. In contrast to other video footage [1], this (silent) movie, filmed at Pavlov’s laboratory, indeed depicts the use of a conventional handbell (Fig. 2). To the best of our knowledge, images from this sequence have never been shown in print. The film was made known to a Western medical audience for the first time in 1928 in New York [2] and, probably††, a second time in 1932 in Rome [22]. In 1960, an- § In this paper (reference [5]), Anrep mentions the use of a “simple bell” as an extra stimulus able to inhibit the inhibition of a conditional response. ** “Professor Pavlov allowed me, for the sake of clarity, to introduce some modifications and additions into the text in order to make the reading lighter for those English and American readers unfamiliar with the original literature in this field. This I have done sparingly, being careful only to expand, but in no sense to alter, the original meaning.” (p. viii) [17] †† According to the opening captions of the 16 mm version, the film was personally projected by Pavlov himself at the 14 th International Physiological Congress [22]: “This film was prepared by and under the direction of Ivan Petrovich Pavlov and was projected by him at the 16th International Congress of Physiology in Rome in 1932. After the congress, Pavlov donated the film to Carlo Foà who was then Professor and Chairman of the Department of Physiology at the University of Milano Medical J Neurol DOI 10.1007/s00415-015-7858-5 ELECTRONIC SUPPLEMENTARY MATERIAL other English version (i.e. a 16-mm copy with English captions) was produced [22]. The movie was also made available to a broad lay audience. It was presented at cinemas from November 1928 (announced in the New York Times [12]) and was released in the USA by Amkino Corp., as an educational film for home projectors, at the latest in 1930 [3]. The latter was described as “the famous Pavlov film” [3] and “a film digest [and] animated photographic record of the experiments and studies of a single individual, Professor Pavlov” [12]. At the Fifth Avenue cinema, New York City, this purely scientific movie, hardly an entertainment, was still playing a month later, suggesting considerable interest on the part of the public [11]; according to the Columbia Daily Spectator, the playhouse was almost sold out [4]. Importantly, however, the short sequence showing the use of a handbell does not depict the generation of a CR but simply illustrates one of the “best known unconditioned [our emphasis] reflexes”, i.e. “the defensive reflexes” as the captions have it, going on to explain: “A response to stimulation mediated through the subcortical centers of the brain is called an unconditioned reflex”. What is shown is simply “the response to a sudden sound“. Only the subsequent sequence depicts the “study of the alimentary unconditioned reflex”; there, a metronome rather than a bell is used as auditory stimulus. In apparent contrast, the then widely read Time magazine reported in 1928: “The process of changing an unconditioned reflex into a conditioned reflex was clearly demonstrated to an audience of psychiatrists at the Academy of Medicine last week, in a cinema entitled 'The Mechanics of the Brain.' School. The film was used in Foà's course of medical physiology in Milano and in Sao Paulo, Brazil, until his retirement. In 1960 the film was brought to Detroit where 16 mm copies were made and the potentially explosive 35 mm original nitrate film was destroyed in compliance with fire safety regulations." – There is no doubt that Pavlov attended the congress. Searching for independent confirmation regarding the presentation of that film, we found an entry in the catalogue of the British University Film & Video Council which lists a film entitled ‘Functions of the Brain: Behaviour of Human and Animal’ (alternative title: ‘Functions of the Brain: Behaviour of Man and Animal, Mechanism of the Brain’) and explains: “This silent film features documentary footage of Ivan Petrovich Pavlov’s laboratory, originally shown in 1932. It shows […] an experiment with children who are fed cookies via a mechanical device to demonstrate conditioned responses; an experiment with a dog that demonstrates alimentary unconditioned reflexes; unconditioned reflex responses and conditioned responses using food, sound or a shock plate. There is also footage comparing child development from a newborn to a sixyear-old”. It seems that ‘Functions of the Brain’ (75 min) is an extended version of ‘Mechanics of the brain’ (1926 version: 35 min; 1928 version: 43 min). The cinema showed dogs which dripped saliva at the sound of a bell (...) if a bell is rung every time the food appears, there will come a time when the dog will secrete saliva at the sound of the bell when there is no food in sight. The simple reflex has been conditioned by the bell; the dog has associated the food with the sound; the power house of the upper brain has gone into action, and the intelligent animal now reacts to an idea.” [2] Conceivably, therefore, a simple mistake by a Time magazine reporter had a formative influence on the iconic commonplace image of Pavlov’s experiments on CC involving a (conventional) bell. While the translation of “звонок” as “bell” by Gantt, and previously by the translators of Pavlov’s 1906 Huxley lecture in The Lancet [19], as pointed out by Todes [25] – may also have contributed to this image, the Time magazine probably reached a broader audience than both Gantt and The Lancet. In summary, it seems from our research into Pavlov’s publications and those of his co-workers that there is indeed sufficient evidence to corroborate the thesis that some sort of bell was at least occasionally employed in CC experiments by Pavlov or his assistants. The statement that a bell was never used [8] may thus be a little too harsh and the ‘dog-and-bell scenario’ described in so many textbooks may indeed have some factual basis. However, we found only very limited evidence from a single drawing that the bell used was indeed a conventional handbell. Moreover, from our screening of Pavlov’s works it seems that other stimuli may have been used more often than a bell. Finally, we suggest that the iconic image of a dog being conditioned by use of a bell may well have been strongly influenced by a verifiably incorrect 1928 report in Time magazine. Conflict of interest The authors declare that they have no conflict of interest. References 1. Ivan Pavlov: Experiments In Conditioning. Uniform resource locator: https://www.youtube.com/watch? v=N5rXSjId0q4. Date accessed: 30th of May 2015. 2. Anonymous (1928) Conditioned Reflex. Time 11:p22-23 (accession number 54758845; last retrieved 54758831 May 54752015) 3. Anonymous (1930) Featured releases, for home projectors. Movie Makers 5:8 4. Anonymous (1928 ) Screenings. In: Columbia Daily Spectator. New York, p 1 5. Anrep GV (1920) Pitch discrimination in the dog. J Physiol 53:367–385 J Neurol DOI 10.1007/s00415-015-7858-5 ELECTRONIC SUPPLEMENTARY MATERIAL 6. Asratyan EA (1978) Иван петрович Павлов. Издательство «НАУКА», Moscow 7. Black SL (2003) Pavlov's dogs: For whom the bell rarely tolled. Current Biology 13:R426 8. Cambiaghi M, Sacchetti B (2015) Ivan Petrovich Pavlov (18491936). J Neurol 262:1599-1600 9. Catania AC (1994) Query: Did Pavlov's Research Ring a Bell? Psycholoquy Newsletter, Tuesday June 7 1994 10. Gaddum JH (1956) Gleb Anrep. 1891-1955. Biographical Memoirs of Fellows of the Royal Society 2:19-34 11. Hall M (1928) The Circus Kid (1928). The Screen; Winter and the Circus. Other Photoplays. In: The New York Times. New York 12. Hall M (1928) Mekhanika Golovnogo Mozga (1926). The Screen; A Scientific Study. In: The New York Times. New York 13. Henry J (1886) In: Scientific Writings of Joseph Henry. Smithsonian Institution, Washington 14. Kelly GR (1978) A last link to Pavlov: W. Horsley Gantt reflects. Arch Gen Psychiatry 35:1474-1478 15. Kupalov PS, Lyman RS, Lukov BN (1931) The relationship between the intensity of tone-stimuli and the size of the resulting conditioned reflexes. Brain 54 16. Littman RA (1994) Bekhterev and Watson Rang Pavlov's Bell. Psycoloquy 5:1 17. Pavlov IP (1927) Conditioned reflexes. An investigation of the physiological activity of the cerebral cortex. Translated by G. v. Anrep. Oxford University Press: Humphrey Milford, London 18. Pavlov IP (1906) The Huxley lecture. Science 24:568-569 19. Pavlov IP (1906) The Huxley Lecture, on the scientific investigation of the psychical faculties or processes in the higher animals. The Lancet 168:911-915 20. Pavlov IP (1906) The Huxley Lecture. On recent advances in science and their bearing on medicine and surgery. British Medical Journal 2:871-873 21. Pavlov IP (1941) Lectures on conditioned reflexes (edited and translated by W. H. Gantt, with the collaboration of G. V. Volborth). International publishers, New York 22. Pudovkin V (1928/1960) Mechanics of the Brain (1960 version with English captures). Uniform resource locator: https://www. youtube.com/watch?v=th0dqf3JVgo. Date accessed: 30th of May 2015. 23. Pudovkin V (1928) Mechanics of the Brain (original Russian version). Uniform resource locator: http://www.youtube.com/watch? v=YTc06C_fIJY. Date accessed: 30th of May 2015. 24. Thomas RK (1994) Pavlov's Dogs "dripped Saliva at the Sound of a Bell". Psycoloquy 5:4 25. Todes DP (2014) Ivan Pavlov: a Russian life in science. Oxford University Press, New York 26. Tully T (2003) Reply: The myth of a myth. Current Biology 13:R426 27. Павлов ип (1952) Лекции о работе больших полушарий головного мозга. Академия Наук Союза ССР, n.p.p. J Neurol DOI 10.1007/s00415-015-7858-5 ELECTRONIC SUPPLEMENTARY MATERIAL Fig. 1 Chamber for studying the conditional reflex (left, inner part; right, outer part) as depicted in Pavlov’s biography (1953/1974), authored by his pupil E. A. Asratyan, the later head of the Institute of Higher Nervous Activity and Neurophysiology founded after the infamous ‘Pavlovian session’ (modified image from [6]). Note the conventional bell (white arrow and inset) that is shown in addition to two metronomes and a light bulb (black arrows). J Neurol DOI 10.1007/s00415-015-7858-5 ELECTRONIC SUPPLEMENTARY MATERIAL Fig. 2 Scene from Pudovkin’s Mechanics of the Brain (1926), recorded at Pavlov’s laboratory in Leningrad. Note the handbell used (arrowhead and inset). Of note, the scene shows an unconditioned response to an auditory stimulus. In another experiment depicted in the same film, a metronome is used as auditory conditioned stimulus.
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