Psychological Bulletin
2003, Vol. 129, No. 2, 171–194
Copyright 2003 by the American Psychological Association, Inc.
0033-2909/03/$12.00 DOI: 10.1037/0033-2909.129.2.171
Biocultural Orchestration of Developmental Plasticity Across Levels:
The Interplay of Biology and Culture in Shaping the Mind and
Behavior Across the Life Span
Shu-Chen Li
Max Planck Institute for Human Development
The author reviews reemerging coconstructive conceptions of development and recent empirical findings
of developmental plasticity at different levels spanning several fields of developmental and life sciences.
A cross-level dynamic biocultural coconstructive framework is endorsed to understand cognitive and
behavioral development across the life span. This framework integrates main conceptions of earlier views
into a unifying frame, viewing the dynamics of life span development as occurring simultaneously within
different time scales (i.e., moment-to-moment microgenesis, life span ontogeny, and human phylogeny)
and encompassing multiple levels (i.e., neurobiological, cognitive, behavioral, and sociocultural).
Viewed through this metatheoretical framework, new insights of potential interfaces for reciprocal
cultural and experiential influences to be integrated with behavioral genetics and cognitive neuroscience
research can be more easily prescribed.
concerted biological and cultural influences (hence, biocultural
coconstructivism) in tuning cognitive and behavioral development
throughout the life span.
Coconstructivism or the related interactionism per se is not new.
Conceptions of environmental, cultural, and behavioral factors
interacting with the biological inheritance of human development
have long philosophical traditions. For instance, Tetens (1777)
assigned extraordinary plasticity to human nature, thus stipulating
opportunities for environmental, cultural, and individual regulation
during life span ontogeny. At the evolutionary phylogenetic level,
St. George Jackson Mivart (1871) suggested that behavioral
changes and adaptation precede and affect natural selection. Modern behavioral researchers of development have also been sensitive
to the interplay between biology and various specific aspects of the
developmental contexts. Conceptually, there is the consensus that
individual ontogeny is hierarchically organized within an open
developmental system that has multiple levels of contexts. Consequently, developmental phenomena need to be investigated by
jointly considering interactions between endogenous and exogenous processes at various levels (e.g., Alexander, 1969; Anastasi,
1958; Baltes, 1979; Baltes & Singer, 2001; Bronfenbrenner, 1979;
Bronfenbrenner & Ceci, 1994; Gottlieb, 1976, 1998; Magnusson,
1988, 1996; Schaie, 1965).
However, a general awareness of coconstructive notions as such
among developmental researchers is not enough in and of itself to
resolve the nature–nurture and mind– brain controversies. In fact,
these debates have again intensified after the publication of two
working drafts of the sequence of the human genome in February
2001 (Lander et al., 2001; Venter et al., 2001). Through the
marketplace of ideas, media and press coverage of the progress in
genomic research are now swinging the age-old pendulums in the
mind of the general public toward genetic and brain determinism
(Kay, 2000; Moore, 2002; Pääbo, 2001). Never has a time been so
in need of reifying biocultural coconstructive conceptions than
today’s genome era.
Integration of experiential and cultural influences into the dayto-day research practices of behavioral genetics (e.g., McGuffin,
Metaphorically speaking, two related pendulums, one swinging
back and forth from nature to nurture and the other from brain to
mind, have been running the clocks of developmental and cognitive inquiries for centuries. Instead of polarizing toward either end,
this review of recent advances in life and developmental sciences
approaches these two age-old debates through the lens of a crosslevel dynamic biocultural coconstructivism. Details of this conception will become clear as the article unfolds. It suffices here to
underscore the key notions of the term: The effects of a series of
interconnected feed-downward (culture- and context-driven) and
feed-upward (neurobiology-driven) interactive processes and developmental plasticity at different levels (hence, cross-level) are
continuously accumulated via the individual’s moment-to-moment
experiences (hence, dynamic) so that, together, they implement
This research was sponsored by the Max Planck Society. I am particularly grateful to Paul B. Baltes. The seed for this article was planted during
the various conversations with him while collaborating on a presentation at
the 108th Annual Convention of the American Psychological Association,
August 2000, Washington, DC. Throughout the process of preparing this
article, I benefited from the many articles Paul B. Baltes suggested to me
and from stimulating conversations on various topics—in particular, his
advocation of biocultural coconstructive influences on life span development with biology and culture both playing active roles. I also thank Tania
Singer for fruitful exchanges on possibilities of cultural influences on the
neuronal bases of social cognition and emotion and feedback on earlier
versions of this article. I would also like to thank Susan Bluck, Elizabeth
Carhart, Michael Carhart, Alexandra M. Freund, Gilbert Gottlieb, Judith
Glück, Tilmann Habermas, Steffen Hillmert, Laura Martignon, Katherine
Nelson, Justin Powell, Jacqui Smith, Paul Verhaeghen, and Qi Wang for
their valuable discussions or comments on earlier versions of the article. I
give special thanks to Julia Delius for her helpful assistance in language
and style editing. Last but not least, special thanks also go to all the
researchers whose work is reviewed in this article.
Correspondence concerning this article should be addressed to ShuChen Li, Max Planck Institute for Human Development, Center for Life
Span Psychology, Lentzeallee 94, Berlin D-14195, Germany. E-mail:
[email protected]
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Riley, & Plomin, 2001), neuroscience (Shepherd, 1991), and cognitive neuroscience (e.g., Gazzaniga, 2000) requires that interactive processes and mechanisms implementing biocultural coconstruction of brain, mind, and behavior at different levels be further
specified. The lack of such specifications, in part, has been one of
the reasons why the nature–nurture and mind– brain debates have
continued (cf. Ingold, 1998; King, 2000). Thus, a further critical
aspect of reifying coconstructive conceptions to help integrate
research from related subfields of developmental and life sciences
is the need for detailed cross-level frameworks with which interactive processes and developmental plasticity across different levels and time scales can be linked and unified.
Goal and Organization of the Review
Taken together, an integral whole of biocultural coconstructive
influences on life span cognitive and behavioral development most
likely are implemented by a series of closely interconnected interactive processes and mechanisms across different levels. Although
there have been attempts to study the nature–nurture and mind–
brain interactions by different strands of developmental and life
sciences, studying them separately misses the dynamic gestalt of
the open developmental system cutting across multiple levels. This
makes the task of integrating cultural and experiential influences
into the research practices of behavioral genetics and neurosciences extremely difficult, as the interconnections between interactive processes and developmental plasticity across different
levels and time scales are not in the foreground of many current
coconstructive conceptions.
To remedy this situation, the task of this review is thus to piece
together reemerging coconstructive conceptions accompanied by
recent findings of developmental plasticity in related subfields of
life and developmental sciences by outlining a cross-level metatheoretical framework to integrate and extend existing conceptions. A unique contribution of the current framework is that it
highlights how interactive processes and developmental plasticity
at different levels are closely connected to each other and unfold
across different time scales. Consequently, together they channel
reciprocal cultural and experiential influences on behavioral, cognitive, and brain development throughout the life span. In principle, biocultural coconstructive conceptions are generalizable to
various domains of human development. In this article, the substantive focus is on cognitive and behavioral development broadly
defined, including basic perceptual and cognitive processes, autobiographical memory, language, behavioral adaptation, and learning. Indeed, physical environment sets boundaries on the human
condition on the evolutionary phylogenetic scale (e.g., Diamond,
1997). However, throughout this review, aside from a few examples involving other species, the focus is on the socioculturally
constructed experiential environment, which plays a more direct
role in individual human ontogeny.
This article contains five main sections. First, a definition of
culture more apt for examining reciprocal biocultural influences on
development is introduced. Second, a cross-level dynamic biocultural coconstructive metatheoretical framework of life span development integrating interactive processes and developmental plasticity across multiple levels and time scales is proposed. In the
subsequent sections, the metatheory is used as a frame to help
piece together recent findings from various subfields of developmental and life sciences by interconnecting interactive processes
across levels. Third, I review reemerging coconstructive conceptions and exemplary empirical findings of developmental plasticity
at various levels that extend beyond the period of child development, specifically highlighting interactive processes and examples
showing reciprocal cultural influences operating on different time
scales corresponding to various levels of developmental plasticity.
Fourth, to address converging evidence from different levels, I
present a summary section of examples of sociocultural influences
on, and subsequently expressed through, language development
and processing. This section is specifically given as a focal illustration of the intimate interconnections between interactive processes and developmental plasticity at various levels unfolding
across different time scales. Last, new insights into possible interfaces for integrating cultural and experiential influences into the
current research agenda and paradigms of behavioral genetics and
cognitive neuroscience are discussed.
A Triarchic View of Culture: Resource, Process, and
Developmental Relevancy
A comprehensive treatment of anthropological theories of culture is not within the purview of this article (interested readers
should see Shweder, 1991; Wertsch, 1985; Wertsch, de Rio, &
Alvarez, 1995). Here, the focus is on a conception that simultaneously highlights three distinct but related aspects of culture that
are of direct relevance for considering the dynamics of biocultural
coconstructive influences on life span development. Previously,
some scholars have criticized the inadequacy of notions of culture
that view it as acting only to supplement and extend biologically
based capacities. The main concern was that such conceptions
could not address the intertwined relations of culture and biology
in the course of human phylogeny and individual ontogeny (e.g.,
Geertz, 1973). Sharing this concern, I define culture in the present
context as ongoing collective social processes that generate social,
psychological, linguistic, symbolic, material, and technological
resources that influence human development via reciprocal mechanisms feeding back into individuals’ moment-to-moment microgenesis, life span ontogeny involving mind– brain interaction, and
human phylogeny involving culture– gene coevolution. Culture
defined as such simultaneously encompasses three conjoint facets:
resource, process, and developmental relevancy.
Culture as Socially Inherited Resources
Culture has most commonly been conceived as a socially inherited combination of human-made material artifacts, knowledge,
values, and beliefs accumulated from the past of a given social
group that functions as a body of resources to coordinate current
human life with each other and with the physical environment
(e.g., D’Andrade, 1996; Herskovitz, 1948; Tylor, 1874). Such a
cumulative process often involves the “ratchet effect” (Tomasello,
1999, p. 5) or “cumulative cultural evolution” (Tomasello, Kruger,
& Ratner, 1993, p. 495), through which modifications to the
inherited body of cultural resources are being progressively made
by individuals of the society over time. Consequently, the inherited
cultural resources become more complex, encompassing a wider
range of adaptive functions. For instance, paper, other writing
materials and tools, books, and variants of printed and electronic
documents are examples of inherited cultural resources accumulated through cumulative cultural evolution. Together they support
BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
intellectual activities in the modern world that comprise both
conceptual (e.g., ideas and knowledge) and material products that
have resulted from technological innovations of the past (e.g., the
inventions of written language, paper, and printing techniques).
If only the resource aspect is emphasized—as is the case in most
generic definitions—then culture is merely the static and passive
product of past civilization that is used to support the current way
of human life. For a conception of culture to join readily with
coconstructive conceptions, the resource-based view of culture
needs to be extended and combined with a process-oriented notion
and a sense of developmental relevancy.
Culture as an Ongoing Social Process
Besides the aspect of culture involving socially inherited resources, culture also has a process-oriented dimension involving
ongoing collective social dynamics (i.e., face-to-face interpersonal
interactions, other social interactions derived from dyadic interpersonal interactions, and shared intentionality) that construct the
shared social reality in present societies (Berger & Luckmann,
1967; Searle, 1995). The processing aspect of culture has been
particularly emphasized in recent research on cognitive engineering of the workplace and interactive minds (e.g., Baltes &
Staudinger, 1996; Hutchins, 1995; Kirsh, 1999). For instance, the
routines, habits, and performance criteria of a given workplace are
not always static across even relatively short periods (i.e., weeks or
months); rather, they are constructed online with the intentions,
thoughts, and behaviors of members in the group affecting each
other to shape the collective “working culture.”
Bringing the collective social processing aspect of culture to the
foreground makes obvious the social interactions taking place in
the individual’s proximal developmental context as part of the
processes mediating cultural influences on brain, cognitive, and
behavioral development. Furthermore, adding the processing aspect also highlights another related feature of culture, namely,
cultural plasticity. The very processes generating cultural resources are themselves pliable and are subject to changes and
modifications continually arising from mechanisms of social interaction, social learning, and other large-scale changes in technology, population, and environmental factors (Baltes & Singer,
2001).
Culture as Developmentally Relevant
One other somewhat implicit but consistent feature in modern
conceptions of culture is its relevancy for individual development.
For instance, Williams (1973) pointed out that many of these
notions arise from terms referring to processes that help organisms
grow. Similarly, Cole (1999) noted that throughout history, culture
entails a concept of promoting development.
In line with the contextual views of culture as an integral part of
the “garden for development” (Cole, 1999, p. 81) or the “developmental niche” (Super & Harkness, 1986, p. 545, 1997; see also
Gauvain, 1995, p. 25, 1998), the view of culture in the present
article is one of a medium including both resources and the
processes generating them, which together edify individual development to minimize the distance between an individual’s attained
and potential levels of performance (Vygotsky, 1978). Highlighting developmental relevancy as distinct from the resource and
process aspects of culture emphasizes the active role and function
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of cultural resources together with the social processes generating
them in individual development. Different cultures (and subcultures) can differ in the level of resources (or opportunities) they
offer for individual development, in profiles of behavioral expressions, in the constellations and processes of interactive minds, and
in their receptivity to modifications by individual behaviors and
new technological advances (Baltes, 2001).
Taking into account these three facets simultaneously (i.e.,
resource, process, and developmental relevancy), culture as defined here is not only the passive product of socially inherited
resources of human civilizations such as tools, technology, language, knowledge, art, customs, values, and beliefs that are accumulated over the past. Rather, it is the “cogenerator” of culture–
gene coevolution during human phylogeny in the long run; and
together with behavioral, cognitive, and neurobiological mechanisms, it is the active “coproducer” of behavioral, cognitive, and
neurobiological development during individual life span ontogeny
at present.
Piecing Together Interactive Processes Across Levels:
A Cross-Level Dynamic Biocultural Coconstructive
Framework of Development
With the triarchic definition of culture in place, I now present a
cross-level metatheoretical framework (see Figure 1) highlighting
concerted biocultural coconstructive influences on life span human
development that are simultaneously embedded within three time
scales (i.e., phylogenetic, ontogenetic, and microgenetic times)
encompassing multiple levels (i.e., sociocultural, behavioral, cognitive, and neurobiological). As a series of interactive processes
embodied in the framework are explained and substantiated
throughout the remaining sections of this article, it will become
clear that the proposed framework helps with conceptualizing
intimate interconnections among reemerging coconstructive conceptions and recent empirical evidence of developmental plasticity
across levels and time scales. Here, a brief overview of key notions
of the framework is first presented.
Key Conceptions of the Cross-Level Dynamic Biocultural
Coconstructive Framework
Individual ontogeny throughout life is seen as a dynamic process that is cumulatively traced out by moment-to-moment experiences and activities taking place at the behavioral, cognitive, and
neurobiological levels on the microgenetic time scale. These
moment-to-moment microgenetic events are couched within (a)
the proximal developmental context involving culturally embedded social interactions and situations on the life span ontogenetic
time scale and (b) the distal context of culture– gene coevolution
occurring on the long-term phylogenetic time scale.
This framework particularly highlights the interconnections between interactive processes and developmental plasticity at different levels occurring on different time scales. This is represented
schematically in Figure 1 by the dynamic joining of the downward
and upward arrows representing interactive processes occurring on
different levels and time scales. Feed-downward influences (i.e.,
cultural influences arising from human phylogeny affecting individual moment-to-moment experiences at the behavioral, cognitive, and neurobiological levels) are implemented through the
culture–individual, culture–situation, and situation–individual in-
Figure 1. Schematic diagram of the cross-level dynamic biocultural coconstructive framework of development, showing that concerted biocultural
influences are implemented through interconnected interactive processes and developmental plasticity across levels and time scales. Dark blue downward
arrows denote culture–individual interaction; purple downward arrows denote culture–situation interaction; brown downward arrows denote situation–
individual interaction; light blue upward arrows denote individual–situation interaction; pink upward arrows denote situation– culture– gene interaction.
The subscripts e, p, and t represent the current epoch, life period, and moment-to-moment microgenetic time, respectively. The notations of these
subscripts ⫾ 1 . . . i indicate the sequences before (–) or after (⫹) the current e, p, or t, where i represents an arbitrary number between 1 and infinity
(e.g., p – 1 ⫽ the previous life period; p ⫹ 1 ⫽ the next life period; p ⫹ i ⫽ a given number of life periods after the current life period).
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BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
teractive processes. Feed-upward influences (i.e., neurobiologically implemented individual cognition and behavior contributing
to collective social dynamics and cultural change) are implemented through the individual–situation, and situation– culture–
gene interactive processes. Feed-downward and feed-upward influences are dynamically joined across different time scales, thus
generating an integral whole of biocultural coconstructive influences on human development.
No doubt that the feed-upward genetic and neuronal influences
have been and will continue to be the prime research emphases of
biogenetics and neurosciences in the new genome era. To balance
emphases on the two strains of biocultural influences, a further
specific task, to paraphrase Gauvain (1995), is to help locate the
feed-downward sociocultural influences in development. Viewed
through the present framework, cultural influences on moment-tomoment microgenesis are implemented through closely linked
interactive processes across different levels and time scales. Their
effects are continuously being integrated into the individual’s
ontogenetic trace and interwoven together with neurobiological
influences to shape the individual’s behavioral, cognitive, and
brain development across the life span. Therefore, not only do
genetic activities and brain functioning offer the necessary biophysical reality for individual cognitive and behavioral operations,
when considered within the broader context and time frame of
culture and biology coevolution, collective cognition and action
generated from participatory interactions (Nelson, 1996) among
individuals create and define culture. Culture, in turn, orchestrates
individual behavioral, cognitive, and brain development and feeds
back to further cultural change and biological evolution. Furthermore, albeit the focus here is on processes generating coconstructive biocultural influences, it should be underscored that individuals need not merely be passive recipients of their biological and
cultural inheritances. Rather, individuals can also be active agents
(Bell, 1968; Lerner & Kauffman, 1985) by participating in making
adaptive decisions (Gigerenzer, Todd, & the ABC Research
Group, 1999) to regulate the way biocultural influences play out in
their life histories (Baltes, 1997).
Extending Related Coconstructive Conceptions With a
Unifying Frame
Three existing coconstructive approaches are at the foundation
of the present framework: (a) the sociocultural contextual approach viewing child development as simultaneously couched
within multiple time scales and heavily involving culturally embedded social interactions (Cole, 1999; Cole & Cole, 1989; Gauvain, 1995); (b) the probabilistic-epigenetic framework emphasizing bidirectional influences among genes, behavior, and
environment (Gottlieb, 1991, 1998, 2000); and (c) the life span
theory of development highlighting exchanges between cultural
and biological resources throughout life (Baltes, 1987; Baltes &
Schaie, 1973; Baltes, Staudinger, & Lindenberger, 1999; Birren,
1964; Nesselroade & Reese, 1973). However, because of the
complexity of the developmental system involving interactions
among multiple levels and time scales cutting across disciplinary
boundaries, research efforts thus far have been local and divisional, missing the dynamic gestalt of such interconnections. For
instance, on the one hand, although bidirectional gene–
environment influences are emphasized, complex human social
situational and cultural linguistic contexts are not within the pur-
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view of the probabilistic-epigenetic framework. On the other hand,
although the sociocultural contextual approach focuses on cultural
influences on social interactions in the individual’s proximal developmental context, interactive processes at the genetic and neuronal levels are not addressed. In addition, both approaches do not
explicitly consider the cumulative developmental history as an
important aspect of the developmental context. Contrary to these
approaches is the life span theory of development, which advocates the culture– biology interplay throughout the life span but
does not address details of the connections between sociocultural,
neuronal, and genetic interactive processes.
Similarly, there have been some other recent attempts at the
local specifications of interactive processes, each addressing a
subfacet of the developmental system. For instance, some researchers have focused on the development of memory and cognition in relation to cultural influences on language development,
because parental speech and culture-specific aspects of language
processing constitute children’s social linguistic environment (e.g.,
Mullen & Yi, 1995; Nelson, 1996; Wang, Leichtman, & Davis,
2000). Others have emphasized the roles of interpersonal relationships in mediating sociocultural influences on child development
at the behavioral (e.g., Reis, Collins, & Berscheid, 2000) and
neurobiological levels (e.g., Siegel, 1999). Some other researchers
have contended that cumulative developmental history constituted
by moment-to-moment experiences is an important developmental
context on its own that leads to specification of functions at the
behavioral (e.g., Thelen & Smith, 1994) and neuronal levels (e.g.,
Johnson, 1999, 2001; Karmiloff-Smith, 1998; Kingsbury & Finlay,
2001). Still, there have been others advocating that child cognitive
(e.g., Bjorklund & Pellegrini, 2000, 2002; Geary & Bjorklund,
2000) and brain development (Finlay & Darlington, 1995; Killackey, 1990; Kingsbury & Finlay, 2001) should be considered
within the larger evolutionary context as subjecting to multiple
shaping forces and selection pressures.
If research continues to be pursued independently with respect
to different development contexts at these different levels, the
dynamic gestalt of the open developmental system involving a
series of closely linked interactions and plasticity across developmental contexts at different levels on varying time scales will not
be obtainable. Integration of sociocultural influences on development into the day-to-day research practices of behavioral genetics
and neurosciences would also be difficult to reify. If interconnections between interactive processes and developmental plasticity
across levels are not readily in view, new insights for potential
interfaces and experimental designs testing relations between processes at different levels are hard to conceive. While being aligned
with previous approaches, the present proposal extends beyond
them by integrating their main conceptions (i.e., different time
frames, multiple levels, and cumulative ontogenetic traces) into a
unifying frame that treats life span development as occurring
simultaneously within multiple time scales and levels. Such integration brings the interconnections between different levels of
developmental contexts currently being investigated by various
strands of developmental and life sciences to the foreground. This
proposal thus provides a unifying framework for investigating how
interactive processes and developmental plasticity at different levels are related to each other and unfold across different time scales,
implementing conjoint coconstructive biocultural influences online throughout life span development.
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Plasticity at All Levels and Reciprocal Cultural Influences
Operating on Different Time Scales
Biocultural coconstructive influences on development as outlined above necessarily imply developmental plasticity at different
levels. Reviewing recent progress in various subfields of life and
developmental sciences, a clear reemerging zeitgeist of coconstructive and related interactive conceptions that are accompanied
by much recent empirical support for developmental plasticity at
different levels1 can be readily gleaned (see summary in the
Appendix). Two examples of the reemerging coconstructivist zeitgeist are highlighted here. In the area of cognitive sciences broadly
defined, coconstructivism has been recently reactivated. For instance, Clark (2001) wrote,
Recent work in neuroscience, robotics, and psychology . . . stresses
the unexpected intimacy of brain, body, and world and invites us to
attend to the structure and dynamics of extended adaptive systems. . . .
While it needs to be handled with some caution, I believe there is
much to be learned from this broader vision. The mind itself, if such
a vision is correct, is best understood as the activity of an essentially
situated brain: a brain at home in its proper bodily, cultural, and
environmental niche [italics added]. ( p. 257)
Advocating the necessity and benefits of integrating cultural and
contextual influences into biological research does not stem only
from the viewpoint of behavioral researchers. In the arena of
neurobiology, Jean-Pierre Changeux (1985) saw the possibility of
“cultural imprint” and stressed the importance of integrating cultural influences into neuroscience research more than 15 years ago:
Writing leaves an impression on the brain, but where? Our lack of
knowledge here does not allow us much room for speculation. We
might expect that many areas are involved. . . . But neurological data
are often hard to interpret; moreover, experimentation is difficult, if
not impossible. Nevertheless, the diversity of human culture provides
fantastically rich material [italics added], and there are a few rare
situations where nature carried out its own experiments, even providing controls! (p. 244)
Developmental plasticity at the various levels corresponds to
interactive processes implementing reciprocal cultural influences
operating on the time scales of human phylogeny, individual life
span ontogeny, and moment-to-moment microgenesis. In what
follows, I present conceptions of coconstructivism and developmental plasticity at different levels with exemplary findings from
the macro- (i.e., evolutionary and cultural changes) to the microlevels (i.e., neuronal and genetic activities). Interwoven among
them are sections highlighting examples of interconnected interactive processes implementing reciprocal cultural influences on
three time scales. Data instantiating culture’s reciprocal long-range
effects on culture–gene coevolution are more of the nature of
historical and population evidence, whereas data supporting socially mediated effects through the proximal developmental context or immediate effects on moment-to-moment microgenetic
experiences are of the empirical nature.
Cultural and Evolutionary Plasticity
At the macrolevel of human phylogeny, there is a growing
interest among researchers of human evolution in the interaction
between biological evolution and cultural change. Increasingly,
researchers have argued that evolutionary approaches to human
behavior and cognition can only be fully appreciated by incorporating an understanding of how human beings, endowed with
cultural inheritance (e.g., marital and socioeconomic institutions
and medical technology), modify significant sources of selection in
their environment (e.g., reproductive success, disease survival
rates, and longevity), thereby codirecting subsequent biological
evolution (e.g., Boyd & Richerson, 1985; Deacon, 1997; Durham,
1991; Feldman & Laland, 1996; Laland, Odling-Smee, & Feldman, 2000; Tomasello, 1999). Along the same lines, Gottlieb
(2002) recently contended specifically that behavioral changes
incurred during development could instigate genetic changes if
transgenerational rearing conditions were relatively stable.
Evolutionary plasticity. Regarding evolutionary plasticity on
the one hand, it has been argued both on empirical and theoretical
grounds that genetic programs and brain organizations reflect the
sociocultural basis of evolution (e.g., Edelman, 1992). For instance, the dairy farming culture selects for adult lactose tolerance
and leads to populations in dairy farming societies with a high
percentage (i.e., over 90%) of lactose absorbers (Aoki, 1986;
Feldman & Cavalli-Sforza, 1989). Or consider as a different example, Dunbar’s (1993) proposition that the biological evolution
of brain encephalization was, in part, driven by the increase of
social group size and the emergence of language as a more efficient means for handling complex social interactions.
Cultural plasticity. On the other hand, culture itself is also
plastic, subject to changes and modifications by individual behaviors, new technology, or population and environmental factors
(Baltes & Singer, 2001). For instance, it has been suggested that
individual learning and experience affect the adoption of cultural
traits (Durham, 1991). The invention of writing led to other inventions such as printing, electronic mailing, and electronically
distributed databases. Subsequently, these could affect the roles of
individual minds and external memory devices and the forms and
styles of knowledge representation and processing, which together
constitute new cultural facets of information transaction and transmission (Donald, 1991; Hutchins, 1995; Laland et al., 2000). For
instance, the popularity of Internet access over the past decade has
already changed the style of academic publishing and many other
aspects of daily life, such as shopping and banking activities
(Eriksen, 2001). In addition to technological development, culture
is also sensitive to other large-scale environmental and population
factors. For example, an increase over the 20th century of average
life expectancy at birth from 45 to 75 years has resulted in the
growing number of aging populations in many developed countries
(Kannisto, 1994). This could lead to modifications in social and
economic policies concerning retirement that, in turn, could affect
the retirement culture and roles of seniors in societies.
1
Outside the immediate realm of developmental research, related interactive conceptions, though not necessarily coconstructive in their emphases, are also embedded in current theories taking cross-level integrative
approaches to memory (Squire & Kandel, 1999), cognition in general (e.g.,
Gazzaniga, 2000), cognitive aging (e.g., Braver et al., 2001; S.-C. Li, 2002;
S.-C. Li, Lindenberger, & Sikström, 2001), and social neuroscience (e.g.,
Cacioppo, Berntson, Sheridan, & McClintock, 2000; Ochsner & Lieberman, 2001), as well as in different variants of a contextualized approach to
situated and embodied cognition and mental universals (Clark, 1999;
Pylyshyn, 2000; Shepard, 1995).
BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
Culture’s Long-Range Effects on Biological Evolution
Corresponding to the evolutionary and cultural plasticity discussed above are culture’s long-range reciprocal effects operating
on the human phylogenetic scale. On this macroscale, these longrange effects themselves are composites of various feed-downward
and feed-upward interactive processes affecting individual ontogeny, social dynamics, and cultural change in the current epoch,
which together modify the sources of natural selection for biological evolution in the next epoch.
For instance, Laland et al. (2000) recently extended conventional coevolutionary theory by postulating a set of mediating
mechanisms called niche construction to relate biological and
cultural changes to each other. Central to the concept of niche
construction is the capacity of organisms and individuals to modify
and construct the sources of natural selection in their environment
by means of (a) learning and experience-dependent processes
during individual ontogeny and (b) processes of cultural change.
These two broad categories of processes of niche construction can
be further dissected as the collective effects of a series of connected interactive processes across different levels and time scales
within the cross-level dynamic biocultural coconstructive framework of development.
Processes for learning and experience-dependent changes involve, in part, direct cultural influences on an individual’s
moment-to-moment activities and experiences. Through an individual’s first-hand personal experiences with the physical or formal properties of culture-specific artifacts and symbolic tools
evolved over the human phylogenetic time (i.e., direct culture–
individual interaction, denoted as the dark blue downward arrows
in Figure 1), culture exerts direct influences on microgenetic
moment-to-moment activities at the genetic, neuronal, cognitive,
and behavioral levels. The phonological and orthographical properties of a language are examples of formal, rather than social
interactive, properties of a given language that through cultureindividual interactions could exert direct influences on the perceptual and neuronal aspects of language processing. There are also
culture–situation interactive processes (i.e., culture–situation interaction, denoted as purple downward arrows in Figure 1) channeling long-term phylogenetic effects to initially shape culturally
embedded social situational contexts involving social customs,
values, interactions, and concepts about individuals and identity.
Subsequently, through situation–individual interactive processes
(i.e., situation–individual interaction, denoted as brown downward
arrows in Figure 1) the influences of culturally embedded social
interactions (e.g., parent– child interaction, schooling, and other
social interactions) on individual life span development are implemented via moment-to-moment experiences and activities taking
place on the microgenetic time scale.
Processes for cultural changes involve individual–situation interactive processes that cumulatively integrate moment-to-moment
experiences at the genetic, neuronal, cognitive, and behavioral
level into an individual’s ontogenetic history (i.e., individual–
situation interaction, denoted as light blue upward arrows in
Figure 1); subsequently, processes of collective social dynamics
played out in the individual ontogenetic histories of a society’s
members generate further culture– gene coevolution (i.e.,
situation– culture– gene interaction, denoted as pink upward arrows in Figure 1).
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Cultural transmission within a social group may homogenize a
population’s behavior. Because culturally transmitted traits can
spread through the population rapidly compared with genetic variants, culture can generate atypically strong selection (Feldman &
Laland, 1996). If cultural changes are rapid relative to transgenerational environmental changes, then the rate of evolutionary
biological changes may be accelerated. Two illustrative examples
of culture’s long-range effects affecting evolutionary biological
changes expressed at the behavioral and physiological level are
given below.
Dairy farming and lactose tolerance. For instance, through the
culture–situation and situation–individual interactions (downward
purple and brown arrows in Figure 1, respectively) dairy farming
culture and other sociocultural influences on the proximal developmental context, such as socioeconomic factors, could affect
infant-feeding customs and the relative ease of getting dairy products. Infant-feeding customs, in turn, can affect the amount of
lactose intake and milk drinking behavior early in and throughout
an individual’s life on the microgenetic time scale. Mediated
through collective social dynamics, these effects could then further
affect socioeconomic influences on dairy farming and customs of
dairy product intakes (i.e., individual–situation interaction, light
blue upward arrows in Figure 1). Collective social dynamics, in
turn, could generate cultural changes and feed back to culture–
gene coevolution in the next epoch (i.e., situation–culture–gene
interaction, pink upward arrows in Figure 1), selecting for individuals with high lactose tolerance. In populations with dairy
farming traditions, the percentage of lactose absorbers often exceeds 90, whereas in populations without such a tradition it is
typically below 20 (Aoki, 1986; Feldman & Cavalli-Sforza, 1989).
Modern urban living and stress resistance. Consider another
example (Diamond, 1997): The development of agriculture did not
only indirectly lead to changes in individuals’ diets and habitats, it
also led to changes in societal structures with increasing social
group size (i.e., an example of culture–situation interaction), which
then affected the psychological and physiological stresses experienced by humans in modern societies on the momentary and daily
bases (i.e., an example of situation–individual interaction). The
increased stress level in modern urban living, in turn, might
influence biological evolutionary changes in the long run. For
instance, the high stress level of modern life could modify the
selection pressure to select for individuals with greater stress
tolerance. Olson (1999) suggested that on the basis of conditional
beneficial phenotype, a “less-is-more” mechanism (i.e., having
less phenotypic expression of anxiety under stress means that one
is more adaptive to high-stress lifestyles) might be invoked in
biological evolution, in which mutations involving the loss or
shedding of sensitive genetic reactions to stress (i.e., the loss-ofgene-function mutation) might occur.
Besides the above examples of long-range reciprocal cultural
influences being supportive for evolutionary biological changes,
there can also be counteractive effects. For instance, late-life
illnesses, such as Alzheimer’s disease, with a sharp prevalence rate
increase among 90 –100-year-olds, illustrate reciprocal environmental and cultural influences that, in part, counteract evolutionary
changes. Given that reproductive-fitness-based evolutionary selection operates primarily in the first half of life, selection benefits
decrease with age. Furthermore, this age-related decrease of evolutionary selection was further enhanced by the fact that environmental and cultural contexts up to the early 1900s allowed a life
178
expectancy at birth of only about 45 years, so that only a small
amount of people in the population reached very old age. Besides
other biological processes of aging, genes and cells active in late
life are more often dysfunctional than those operating early in life.
Given that evolutionary selection cannot operate as frequently
regarding maladaptive phenotypic characteristics expressed in late
life as in earlier life periods, dysfunctional late-life genes are not
likely to be selected against during biological evolution (Finch,
1990; Hayflick, 1998; Martin, Austad, & Johnson, 1996).
Behavioral and Cognitive Plasticity
Regarding the next level of the framework, namely, individual
ontogeny, various theories in the area of developmental psychology have emphasized the malleability of behavior and cognition by
cultural, social, and learning factors (see Collins, Maccoby, Steinberg, Hetherington, & Bornstein, 2000; Lerner, 1998, for reviews).
For instance, Vygotsky (1978) had already emphasized the role of
social interactions in proximal developmental contexts such as
parent– child relation, peer relation, and schooling in promoting an
individual’s attained level of development toward a higher level of
potential. More recently, sociocultural contextual approaches have
been promoted (e.g., Cole, 1999; Cole & Cole, 1989; Gauvain,
1995) that focus more specifically on cultural influences affecting
these social interactions and their subsequent mediated effects on
individual development. In a related but different vein, rather than
focusing on cultural influences at a higher level, the relationship
contextual approach (e.g., Reis et al., 2000) examines fine-grained
details (e.g., emotional and cognitive aspects) of different types of
interpersonal relationships and their impact on child development.
Still other researchers have focused on the linguistic environment
as a main facet of culture-specific social interactions in an individual’s proximal developmental context (e.g., Engelkamp, 1978;
Mullen, 1994; Nelson, 1996).
Cross-cultural studies on parenting style (Bornstein, Tal, &
Tamis-LeMonda, 1991) found that differential emphases on interpersonal versus object orientation mediated through parent– child
interactions in the Japanese and American cultures, respectively,
affected the types of languages and games (or playing) at which
the toddlers in these two societies performed well. In the aspect of
schooling, cultural differences in the emphases of teachers’ instructions were shown to affect the acquisition of metacognitive
skills such as memory and computational strategies (Rogoff,
1990). It has also been suggested that the differential emphases of
holistic versus analytical thinking in the East Asian and Western
cultures, respectively, are associated with the individuals’ causalattribution style. In this case, analytical thinking style was found to
be related to a greater propensity in American individuals to
interpret behavior as the direct result of dispositions corresponding
to the apparent nature of the behavior itself. The greater tendency
of East Asians to include background, contextual, and relational
information in their causal-attribution processes could, in part, be
attributed to their holistic thinking style (e.g., Choi, Nisbett, &
Norenzayan, 1999; Norenzayan & Nisbett, 2000).
In terms of cognitive plasticity in old age, memory training
studies (Baltes & Kliegl, 1992) showed that older adults (aged
from about 60 to 80 years) still displayed a fair amount of cognitive plasticity. They could improve memory recall by up to 10
words by using a culture-based mnemonic technique (i.e., method
of loci), notwithstanding the usual average memory span of about
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five words for individuals in this age range. Further evidence
suggests that marginal cognitive plasticity is still preserved, to
some extent, in very old age, allowing older adults in the “fourth
age” (i.e., aged 80 years and older) to benefit from being informed
about the mnemonic technique (e.g., Singer, Lindenberger, &
Baltes, in press). There is also evidence for adaptive behavioral
plasticity compensating for the decline of processing resources in
old age. For instance, falling has a greater nonadaptive consequence for older than young adults. Older adults’ more frequent
use of walking aids rather than memory aids in a dual task
involving memorization and walking, indicating that they were
able to adaptively devote less effort to memorization and more to
concentration on walking so as to keep themselves from falling
(K. Z. H. Li, Lindenberger, Freund, & Baltes, 2001). These findings together indicate that cognitive and behavioral plasticity are
among the hallmarks of individual life span development.
Culture’s Midrange Effects on Ontogenetic Behavioral
and Cognitive Development
Corresponding to behavioral and cognitive plasticity are culture’s midrange effects implemented through culture–situation interactive processes that affect individuals’ behavior and cognition
during ontogeny. Cross-cultural differences in parental styles,
schooling, and other norms of social interaction, such as socialization goals and self-construal, reveal the cultural influences
accumulated thus far over phylogenetic time on social interactions
in the current proximal developmental context of an individual
(i.e., culture–situation interaction). Effects of these culturally embedded social interactions on development are then implemented
by the behavioral, cognitive, neurobiological, and genetic activities
on the scale of microgenesis involving moment-to-moment experiences and activities (i.e., situation–individual interaction). In the
following sections I provide examples of cultural influences on
activity goals that subsequently affect infant sleeping behavior and
of cultural influences on schooling that subsequently affect metacognitive styles.
Intergenerational transmission of activity goals and infant
sleeping behavior. Concrete examples of cultural influences implemented through culture–situation interactive processes shaping
social interactions in the proximal developmental context involve,
for instance, the collective goals and values shared by members of
a given culture affecting the way individuals conceive their own
life goals. This, in turn, affects the organization of daily planning
and behavior. For instance, cultural shift caused by industrialization led to a reorganization of cultural practices with respect to
time schedules. Thus, one aspect of becoming modern was behavioral change toward a greater sensitivity to planning activities in
advance (Inkeles & Smith, 1974). Such general cultural shifts in
goals and values may subsequently be transmitted into individual
behavior and cognitive development via proximal influences involving parent– child interaction and other social learning mechanisms (Bronfenbrenner & Ceci, 1994; Cole, 1999; Collins et al.,
2000). As an illustration, consider a study by Super and Harkness
(1997) demonstrating how different societies’ cultural practices of
timing and scheduling are transmitted and expressed in young
infants’ sleeping patterns through parent–infant interaction and
customs of child care. American urban-dwelling infants whose
parents had jobs outside the home and lived by tight working
schedules, developed a marked shift toward the adult day–night
BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
cycle shortly after birth. By the end of the second week, American
urban babies slept an average of about 8.5 hr between 7 p.m. and
7 a.m. In contrast, the longest period of sleep reported in a sample
of rural Kenyan (Kipsigis) infants was only 3 hr. In comparison
with American urban culture, rural Kenyan culture places much
less emphasis on strict scheduling. During the day the Kipsigis
babies napped a lot while strapped to their mothers’ backs, accompanying them going about their daily activities. During the night
Kipsigis babies slept with their mothers and were nursed whenever
they were hungry. Therefore, the Kipsigis babies did not need to
adapt quickly to a rigid adult day–night cycle. Indeed, the Kipsigis
babies’ longest sleep episode increased little over the first 8
months of infancy.
Schooling and metacognitive styles. Besides parent– child and
other close interpersonal relationships, other forms of social learning, such as schooling, also serve as a channel to implement
cultural influences on metacognitive styles (Rogoff, 1981, 1990).
For instance, one study (Carraher, Carraher, & Schliemann, 1985)
found that for Brazilian child street venders, doing arithmetic had
a socioeconomic context with clear business goals. When the
context of mathematic activities and the goal of calculations were
meaningful with respect to the sociocultural context, the Brazilian
junior street businessmen’s computations were more successful
than when they did the pure arithmetic derivations in classroom
settings common in many other societies.
In other cross-national studies, Carr, Kurtz, Schneider, Turner,
and Borkowski (1989) showed that memory strategy instruction
varied across different education systems and led to cross-national
differences in memory performance. Specifically, these authors
found that German and American teachers differed in the type of
memory strategy instructions they gave in classrooms. This difference was paralleled by the German school children’s higher
levels of memory recall and memory organizational strategies in
terms of sorting and clustering than their American peers, before
systematic strategy training was administered to both groups.
Situation–individual interactive processes channeling the above
intergenerational-, interpersonal-, and schooling-mediated cultural
influences on individual development are executed in moment-tomoment experiences and activities occurring on the microgenetic
time scale involving the behavioral, cognitive, and neurobiological
levels. Research on mechanisms subserving cultural and social
learning through microprocesses of interpersonal interactions, such
as the ability to mentally represent and predict other people’s
intentions and behavior (i.e., the ability to have a theory or simulation of another’s mind) and associated processes of shared gaze
and joint attention, has already begun (e.g., Baron-Cohen, 1995;
Carpenter, Nagell, & Tomasello, 1998; Frith & Frith, 1999). I
discuss other interactive processes implementing culture’s immediate effects on different levels of moment-to-moment experiences
after first presenting empirical findings of neuronal and genetic
plasticity.
Neuronal Plasticity
In the field of neurobiology, since the discovery of long-term
potentiation (Bliss & Lømo, 1973)—long-lasting increase in the
synaptic strengthening between simultaneously firing pre- and
postsynaptic neurons—which affirmed one aspect of Hebb’s
(1949) principle regarding repeated simultaneous firing, neuroscientists have been investigating behavior- and experience-
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dependent neuronal plasticity. After Hebb’s proposal, both the
selective stabilization theory of neuronal epigenesis (Changeux,
1985; Changeux & Danchin, 1976) and the neuronal group selection theory (Edelman, 1987; Edelman & Mountcastle, 1978) further supported the notion that the details of cortical organization
are affected by developmental and experiential influences. Since
then, many empirical findings have shown that various brain
regions exhibit experience-dependent structural plasticity (i.e.,
changes in synaptic connectivity and the generation of new neurons) and changes in functional cortical circuits (i.e., cortical
functional plasticity).
Structural plasticity. It has been demonstrated that the brains
of rats reared in environments enabling broader ranges of behaviors and experiences also show more mature synaptic structure
with more synapses per neuron than rats reared in less stimulating
environments (Black & Greenough, 1998; Greenough & Black,
1992; Rosenzweig, 1996). In humans, it was recently demonstrated
that the overall cortical gyral patterns, though in part affected by
genes (e.g., Pennington et al., 2000), could also be influenced by
nongenetic experiential factors (Bartley, Jones, & Weinberger,
1997). Another example focuses on the amygdala, a brain region
that is very much involved in social– cognitive neurodevelopmental disorders (e.g., autism) and is sometimes referred to as the
innate module for the development of social cognition (e.g.,
Baron-Cohen, 1995) and emotion (e.g., Öhman, 2002). Contrary to
the innate notion, although the amygdala nuclear complex develops relatively early in human gestation (Embryonic Day 30 to 50),
the separate nuclei do not start to differentiate until after birth,
suggesting plasticity in the amygdala’s responses to experiential
influences (Kordower, Piecinski, & Rakic, 1992).
Functional plasticity. Aside from plasticity in synaptic connectivity, structures, and gyral patterns, neuronal processes also
exhibit functional plasticity. For instance, the sensorimotor cortex
in blind individuals develops a larger representation corresponding
to the Braille-reading finger and shows cross-modal plasticity in
terms of reorganization in the visual cortex for tactile and auditory
information processing (for reviews see Hamilton & PascualLeone, 1998; Kujala, Alho, & Näätänen, 2000). Or consider another example of a reversed phenomenon: In congenitally deaf
individuals, visual processing dominates parts of the cortex that are
usually involved in auditory function (Neville, 1991; Neville &
Lawson, 1987).
Cumulative Developmental Influences on Neuronal
Plasticity Across the Life Span
One salient aspect of the evidence on neuronal plasticity shows
that cortical plasticity also reflects the influence of cumulative
developmental history across the life span. A developing brain is
more uniform and lacks the specificity of a developed adult brain.
Accumulating data suggest that the functional specialization of the
neocortex is established through subsequent epigenetic interactions with the immediate experiential environment (Changeux,
1985; see also Johnson, 2001; Kolb & Whishaw, 1998; O’Leary,
1996, for reviews). Thus, experiential and cultural influences leave
traces in developing brains, capturing developmental effects accumulated through the individual’s moment-to-moment activities
and experiences. For instance, recently it has been demonstrated
that face processing is less localized or specialized (i.e., not as
differentiated) in infants than in adults. In infants, face processing
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involves both left and right ventral visual pathways, whereas in
adults face processing primarily involves the right ventral visual
pathway. While adult brain activity shows specific sensitivity to
upright human faces, no such sensitivity for face orientation is
observed in young infants (de Haan, Humphreys, & Johnson,
2002; de Haan, Pascalis, & Johnson, 2002).
Furthermore, there is also increasing evidence for cortical plasticity extending beyond the developing brain to all periods of the
life span (summarized in Table 1). Many recent data show that the
adult brain can also adaptively change its structural and functional
organization in response to accumulated developmental history,
thereby reflecting daily experiences and aging. For instance,
Maguire et al. (2000) found that given their extensive navigation
experience, London taxi drivers’ posterior hippocampi, a region of
the brain involved in storing spatial representation of the environment, were significantly larger in comparison to controls of the
same age. Furthermore, when comparing among drivers, the number of years spent as a taxi driver correlated positively with
hippocampal volume. These data indicate that the brain continues
to possess functional plasticity in adulthood, allowing the posterior
hippocampus to expand regionally to accommodate elaboration of
environmental spatial representation in individuals who rely
heavily on their navigation skills and who have achieved a high
level of navigation expertise in a particular environment. There is
also evidence with respect to language processing: Recent event-
related potentials (ERP) studies have demonstrated changes in
cerebral activity in adults following speech discrimination training
or visual word or verbal association learning (e.g., Abdullaev &
Posner, 1997; Kraus et al., 1995; McCandliss, Posner, & Givon,
1997). In terms of language impairment, adult patients who had
recovered from aphasia following strokes showed shifts in language lateralization. Specifically, typical Wernicke’s aphasia patients displayed a shift of function to the right hemisphere that was
long lasting, whereas patients with Broca’s aphasia displayed a
transient shift to the right hemisphere that was followed by a return
to left laterality (Thomas, Altenmüller, Marchmann, Kahrs, &
Dichgans, 1997). Cortical representational restructuring of sensorimotor cortex after limb amputation (e.g., Merzenich, Crajski,
Jenkins, Recanzone, & Peterson, 1991) and compensatory activation of the right prefrontal cortex to preserve language function
after brain damage (e.g., Buckner, Corbetta, Schatz, Raichle, &
Petersen, 1996) have also been observed in adults.
As for functional plasticity during aging, a series of recent
neuroimaging data suggests that cortical information processing in
different regions of the brain becomes less differentiated with
aging. Compared with young adults, who exhibit more clearly
lateralized cortical information processing, people in their 60s and
beyond showed bilateralized (bihemispheric) activity during memory retrieval (e.g., Cabeza, 2002; Cabeza et al., 1997) and during
both verbal and spatial working memory processing (e.g., Reuter-
Table 1
Experience and Life-History-Dependent Cortical Plasticity Across the Life Span
Study
Finding
Childhood
Neville & Bavelier (1998)
Elbert et al. (1995)
Cheour et al. (1998)
Early bilinguals (⬍ 7 years) showed overlapping cortical activation
for native and second language, whereas late bilinguals did not.
Individuals who learned to play string instruments early showed
enlarged cortical representation of the left playing hand.
Language-specific memory traces developed in infants at 12
months.
Adulthood
Hamilton & Pascual-Leone (1998)
Maguire et al. (2000)
Karni et al. (1995)
Blind individuals developed larger sensorimotor representation
corresponding to the Braille-reading finger.
There is evidence of recruiting in the visual cortex for tactile
information processing.
The size of posterior hippocampi was enlarged in individuals, such
as taxi drivers, who relied heavily on navigation skills in daily
activities.
Extensive training of complex finger motor sequences increased
the extent of primary motor cortex activation, suggesting slowly
evolving, long-term, experience-dependent reorganization of the
adult primary motor cortex.
Old age
Cabeza (2002); Reuter-Lorenz et
al. (2000)
Kempermann et al. (1997)
H. Nakamura et al. (1999); Saito
et al. (1994)
Note.
Aging increases bilateral cortical activation in various cognitive
processes, indicating reduced hemispheric asymmetry in older
adults.
Enriched environment induced neurogenesis in the hippocampus of
older rats and improved memory performance.
Enriched environment restores aging-related decrease of
synaptophysin content in older rats by enhanced packing density
of synaptic vesicles in synapses.
All data are human data, except two sets of results indicated in the table.
BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
Lorenz et al., 2000). It has been suggested (Cabeza, 2002; ReuterLorenz, 2002; Reuter-Lorenz et al., 2000) that these data might
indicate that the aging brain could “recruit” cortical areas in both
hemispheres to compensate for neurocognitive declines during
aging.
Regarding structural plasticity in old age, neuroscience’s
century-old dogma that there is no addition of new neurons in the
adult mammalian brain has recently been revised (see Gross, 2000,
for a review). There is now evidence showing that increased
environmental complexity stimulates the growth of new hippocampal neurons (i.e., neurogenesis) in the adult brains of various
species, such as birds (Barnea & Nottebohm, 1994), rodents (Kempermann, Kuhn, & Gage, 1997; Nilsson, Perfilieva, Johannson,
Orwar, & Eriksson, 1999; van Praag, Christie, Sejnowski, & Gage,
1999), and humans (Eriksson et al., 1998).
In summary, cultural influences could have effects on the
brain’s structural and functional organization through early
experiential tuning of synaptic connections and functional circuitry. In addition, though less flexible than in the earlier
periods of development, there is still marked cortical plasticity
throughout most of the adult life span, both in terms of functional plasticity and neurogenesis. This opens up possibilities
for cultural and experiential influences to be intimately integrated into an individual’s cumulative developmental history,
allowing for lifelong adaptations to both ongoing life experiences couched in the individual’s own respective sociocultural
context and life span developmental changes in the efficacy and
integrity of the brain itself.
Genetic Plasticity
I now turn to the genetic level of the proposed framework. In the
field of biogenetics research there has been a recent shift from the
traditional view of unidirectional gene3protein information flow
(Crick, 1958, 1970) to a probabilistic-epigenetic framework emphasizing bidirectional interactions among genes, neuronal activities, behavior, and environment (Gottlieb, 1991, 1998, 2000).
Thus, genetic activity is not viewed as encapsulated and void of
environmental and behavioral influences; rather, there are reciprocal coactive influences between levels. Environmental and experiential influences on genetic activities and expressions have
been found in many empirical studies (see summary in the Appendix; reviews in Gottlieb, 1998). Two examples highlighting
developmental plasticity in relation to feed-downward influences
at the genetic level are given here.
The acquisition of species-specific songs in songbirds illustrates
developmental plasticity implied by feed-downward phylogenetic
influences on moment-to-moment activities at the genetic level. In
songbirds, species-specific songs that are present in the environment stimulate the activation of a set of genes in the forebrain to
further regulate the expression of other genes in the same region
(Mello, Vicario, & Clayton, 1992). Consider also Suomi’s (1999)
finding that maternal style interacted with genetic effects on infant
Rhesus monkeys’ reactions to stressors, which illustrates genetic
plasticity reflecting the effects of feed-downward influences on
moment-to-moment activities at the genetic level that are mediated
through parent– child interactions.
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Culture’s Immediate Effects on Moment-To-Moment
Experiences
On the time scale of microgenesis, either through direct culture–
individual or mediating culture–situation and situation–individual
interactive processes (see Figure 1), culture exerts immediate
effects on moment-to-moment experiences and activities at the
behavioral, cognitive, neuronal, and genetic levels. Regarding cultural influences implemented through direct culture–individual
interactions, the following examples show that individuals’ firsthand personal experiences with the physical or formal properties
of culture-specific artifacts, linguistic, and symbolic tools are
possible channels for culture to exert its direct immediate reciprocal influences on cognition and behavior.
Direct influence of culture-specific artifacts on mental calculation. As discussed previously, the metacognitive aspects of math
skill learning (i.e., strategy use) involve culture–situation interactive processes mediating cultural influences on educational system
and schooling. The physical properties of culture-specific artifacts
themselves, however, could have direct effects on moment-tomoment experiences affecting online cognitive processing by setting specific processing requirements (an example of direct
culture–individual interaction). Consider the example of children
skilled at using an abacus (a once common tool of computation
formerly used daily in East Asian societies) who develop visualized representations of a mental abacus while doing mental calculation. The abacus is a three-dimensional object requiring visual
processing (and also sensorimotor processing at the early acquisition stage). The visualization of a mental abacus not only enhances
the children’s mental calculations but also improves their performance in tasks that require visuospatial processing (Hatano, Miyake, & Binks, 1977; Stigler, 1984), such as backward serial recall
(S.-C. Li & Lewandowsky, 1995). However, at the same time they
are also more susceptible to visuospatial distractors (Hatano,
Amaiwa, & Shimizu, 1987).
Direct influences from formal properties of linguistic or symbolic tools on digit memory and digit and letter processing.
There is also evidence for linguistically mediated cultural influences on numerical memory span. For instance, the quicker pronunciation of number words in the Chinese language appears to
contribute to the digit span advantage in Chinese individuals over
Americans (Geary, Bow-Thomas, Fan, & Siegler, 1993; Stigler,
Lee, & Stevenson, 1986). Likewise, more recent experiments show
that besides the ease of pronouncing number words, Chinese
preschoolers’ advantage over American preschoolers in the ability
to count from 11 to 20 can be related to the more obvious
(10-based) structure of number names in Chinese than in English
(Miller, Smith, Zhu, & Zhang, 1995).
In addition, other culture-based symbolic tools could also affect
cognitive processing. For instance, one recent study (Polk & Farah,
1998) found that even a rather nonsalient aspect of cultural practice, namely, the composition of postal codes, affected individuals’
letter and digit processing. Canadian postal codes are a mixture of
both digits and letters (e.g., V6K 2E8), and in comparison with
their fellow postal workers who did not sort mail, Canadian mail
sorters showed less behavioral evidence for segregated letter and
digit processing. At the neurobiological level, the study found
evidence for dissociated digit and letter processing, with the area
of left inferior occipitotemporal cortex responding significantly
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more during a letter recognition task than during a digit recognition task.
An intriguing question is whether there are also traces of cultural influences on behavioral and cognitive experiences to be
found at the neurobiological level. The following examples provide initial answers.
Direct cultural influences captured by neuronal plasticity. Besides influences channeled through the physical or formal properties of culture-specific artifacts, linguistic, or symbolic tools on the
cognitive level as discussed above, there is evidence showing that
behavioral learning experience with respect to other culturerelevant activities, such as music training, leads to experiencedependent cortical functional reorganization. Elbert, Pantev, Wienbruch, Rockstroh, and Taub (1995) found that cortical
representations of the fingers of the left playing hands of string
players were larger than those of the right hand holding the bow,
and this was particularly true for individuals who started playing
the instrument early in life. Another more recent neuroimaging
study (Ohnishi et al., 2001) compared expert musicians with
nonmusicians and found that while listening to J. S. Bach’s Italian
Concerto, nonmusicians who were not familiar with classical
music showed activity primarily in the secondary auditory association area in the right temporal cortex. The musicians, however,
also showed activities in the auditory association area in the left
temporal cortex and in the left posterior dorsolateral prefrontal
cortex, the brain regions associated with language processing and
working memory functions, respectively.
Parental style- and social interaction–mediated influence captured by genetic plasticity. Feed-downward situation–individual
interactive processes (e.g., parent– child interaction and other social situational contexts) implement mediating effects on the individual’s moment-to-moment experiences that are, in some cases,
also expressed at the genetic level. Consider again here the example of maternal style interacting with genetic effects on the infant’s
reactions to stress. Genetically highly reactive Rhesus monkey
infants raised by especially nurturant females exhibited much less
deficit in early exploration and less accentuated responses to mild
stressors that were otherwise typical for genetically highly reactive
infants raised by normal or highly reactive females (Suomi, 1999).
Furthermore, evidence has been found of transient, non-learningbased social psychological stress interacting with mRNA activity
in the human immune system (Glaser et al., 1990), and, for another
example, Malarkey et al. (1996) found that social stressors are
related to the concentration of lymphocyte growth hormone in late
adulthood. Specifically, caregivers of spouses with Alzheimer’s
disease showed markedly down-regulated growth hormone gene
expression.
In summary, couched within the context of the cross-level
dynamic biocultural coconstructive framework, findings of developmental plasticity at various levels (i.e., evolutionary, cultural,
behavioral, cognitive, neuronal, and genetic plasticity) reflect the
effects of coconstructive interactive processes between biology
and culture that dynamically take place across levels and time
scales. The closely interconnected interactions and plasticity
across levels, thus, form an integral whole of biocultural coconstructive influences on human development. Together, the existing
pieces of empirical evidence present a clear warning against the
pure reductionist approach to the genetic and neuronal bases of
mind and behavior, which ignores the influences from cultural,
experiential, and cumulative developmental contexts. Genes and
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the brain are themselves open systems endowed with remarkable
plasticity to be molded by external and experiential influences as
individuals behave and function throughout life in their respective
sociocultural environments, which are superimposed on the physical environments and embedded in the long-term human phylogenetic time scale (cf. Edelman, 2001).
Connecting Interactive Processes Across Levels and Time
Scales: Converging Evidence From Language Research
Although currently available findings regarding cognitive and
behavioral development as reviewed in the previous section still
leave some gaps between levels and time scales, developmental
plasticity and interactive processes at the multiple levels may be
more closely related to each other than is readily apparent. Findings from research on language, unlike those from research on
other aspects of cognitive and behavioral development, cover a
wider range of levels and time scales. Converging evidence with
respect to sociocultural influences on, and expressed through,
language development and processing at most levels and on different time scales recently has emerged (cf. Kuhl, Tsao, Liu,
Zhang, & de Boer, 2001). In this section, I thus give examples
involving language to focally illustrate that the various interactive
processes and developmental plasticity at different levels as
outlined in the cross-level dynamic biocultural coconstructive
framework are tightly related with each other, unfolding across
the time scales of human phylogeny, individual ontogeny, and
microgenesis.
Coevolution of Language, Group Size, and Brain:
Reciprocal Cultural Influence During Human Phylogeny
Situation– culture– gene and culture–situation interactions operating across the human phylogenetic and individual ontogenetic
time scales are both central to the coevolution of language, group
size, and brain. Focusing predominantly on the human phylogenetic scale, Dunbar (1993) showed that group size covaried with
relative neocortical volume in nonhuman primates. This led to the
proposal that the encephalization of primate brains is not driven by
the cognitive demands of tool making but by an intricate coevolving process between the growth in social group size and the
development of language as a more efficient method for social
bonding (Dunbar, 1998). The subsequent effect on the level of
individual ontogeny, in turn, was for language to become one of
the socially inherited, species-specific cultural resources that support individuals’ interactions with each other and with the environment. Indeed, the linguistic relativity theory (Saunders & van
Brakel, 1997; Whorf, 1956) contends that human understanding of
the world is in part constructed through language.
Brain encephalization is also correlated with the extended juvenile period, a phenomenon that possibly also arose from social
selection pressures involved in managing complex and dynamic
social environments (Bjorklund & Pellegrini, 2000, 2002; Joffe,
1997). The extended juvenile period in humans, then, allows an
extended amount of time and opportunities for intergenerational
social interactions, operating in conjunction with language, to
mediate cultural influences on other aspects of cognitive and
behavioral development during individual ontogeny. To illustrate
this, I provide a few such examples in the following section.
BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
Intergenerational Transmission of Self-Construal, Parental
Speech, and Autobiographical Memory: Reciprocal
Cultural Influence During Individual Ontogeny
One important aspect of culture–situation interactions on individual development is the culture-specific language environment,
whose effects on an individual’s language and cognitive development are mediated through social interactions. Together with
culture-specific characteristics of social interactions, languagespecific differences constitute a unique social linguistic environment as part of the proximal developmental context for individuals
in different cultures. They affect language and other cognitive
development during individual ontogeny. Current evidence
shows that cultural differences in terms of how the self is construed (e.g., the Western independent vs. the Asian interdependent
concept of self; Gardner, Gabriel, & Lee, 1999; Markus &
Kitayama, 1991) and language-specific differences in syntax may
affect the patterns of adult– child interactions, which subsequently
have implications for language development and autobiographical
memory.
For instance, Japanese and American children do not differ in
their language and play skills in general; however, the difference
between the two cultures’ maternal styles of interacting with their
infants, either emphasizing more interpersonal dependence (Japanese) or individual independence (American), is related to the
kinds of languages and play skills the infants later develop as
toddlers (e.g., Bornstein et al., 1991). Moreover, another study by
Gopnik, Choi, and Baumberger (1996) shows that languagespecific differences influence parental speech and subsequently
affect patterns of semantic and cognitive development. For example, English has a highly analytic structure, with relative little
reliance on morphological variation. Nouns are generally obligatory in English sentences, and it is rare to construct sentences
consisting of only an inflected verb without nouns or pronouns.
English-speaking parents thus focus heavily on object naming in
conversations with their children. In contrast, the Korean language
has rich verb morphology, with different verb endings marking
important semantic distinctions. Korean parental speech thus often
consists of highly inflected verbs with few nouns. These authors
found that these culture-specific language differences transmitted
through the parental linguistic environment show subsequent impacts on semantic and cognitive development. Whereas the semantic and cognitive abilities of understanding plans and object categories developed, on average, at roughly the same age for the
English-speaking children, the Korean-speaking children showed a
different pattern. For the Korean-speaking children, means– ends
abilities and verbs that are relevant to the concepts of planning
emerged clearly and consistently before categorization abilities
and nouns that are relevant for grouping objects (Gopnik et al.,
1996).
In a related vein, there have been historical thoughts and contemporary studies on the tripartite relation between cultural and
experiential influences on language, the concept of self, and autobiographical memory. Consider the following excerpt from a historical text by Bernard Connor (1697/2001):2
In the forests between Russia and Lithuania a boy of about ten, who
lived among the bears, was found in 1694. He gave no sign of reason,
walked on hands and feet, had no language, and formed sounds that
had nothing in common with human sounds. It took a long time before
he could utter a few words, which he still did in a very barbarous
183
manner. As soon as he could speak, he was asked about his former
state. But he could not remember any more than we can recall what
happened to us in the cradle [italics added]. (p. 84)
Indeed, recent empirical studies show cross-cultural differences
in autobiographical memory, illustrating cultural effects on selfrelated memory mediated through the culture-specific social linguistic environment. Adults engage children in processes of coconstructing memories by explicitly guiding them during
conversations, thereby helping them produce verbal accounts of
their experiences (Eisenberg, 1985; Nelson, 1993). The more interdependent construal of the self in Asian societies seems to relate
to a lesser need for elaborated autobiographical narratives, which,
in turn, affect early linguistic experiences through parent– child
interactions. For example, Mullen and Yi (1995) found that the
frequency with which Korean mother– child dyads engaged in
conversations about past events was only about one third of that of
U.S. Caucasian mother– child dyads. Wang et al. (2000) compared
American and Chinese mother– child dyads and found that the
Chinese dyads more often used low-elaborative and interdependently oriented conversation styles than the American dyads.
These early linguistic experiences mediated through cultural influences on self-concept permeate parent– child dynamics and, in
turn, underlie cross-cultural differences in adult autobiographical
memory. The average age of U.S. Caucasian adults’ at their
earliest childhood memories was about 3.5 years, whereas for the
Asian adults, it was at about 4 to 4.5 years (Mullen, 1994; Wang,
2001).
Taken together, during individual ontogeny cultural influences
on an individual’s social linguistic environment that are expressed
through cross-cultural differences in intergenerational social dynamics and language-specific differences affect other aspects of
cognitive and behavioral development. Cross-cultural differences
in language syntax influence parents’ style of speech, which later
affects children’s cognitive and semantic abilities (Gopnik et al.,
1996). Regarding the level of narrative contents, cultural differences in how the self is construed affect the content of coconstructed narratives between parents and children about the self,
which subsequently affect the encoding of self-related memory in
early childhood (Markus & Kitayama, 1991; Mullen, 1994). The
fact that this effect later reveals itself as a cross-cultural difference
in the average age of earliest autobiographical memory recalled by
individuals in adulthood indeed signifies that cultural and experiential influences are carried cumulatively throughout the life span.
Direct Language-Specific Influences on Moment-ToMoment Experiences at Multiple Levels: Reciprocal
Cultural Influences on the Microgenetic Scale
The above-mentioned socioculturally mediated influences on an
individual’s linguistic environment are subsequently implemented
by moment-to-moment experiences on the time scale of microgenesis and may leave traces at the perceptual and neurobiological
levels. Empirical findings corresponding directly to the behavior
data regarding the style of parental speech, language development,
and autobiographical memory are not yet available. Nonetheless,
2
I thank Michael Carhart at the Max Planck Institute for the History of
Science, Berlin, Germany, for pointing out this historical text recounted in
his manuscript of a forthcoming book (Carhart, 2002).
184
there are now many data showing the influences of formal properties of language on moment-to-moment experiences at the perceptual and neuronal levels.
Effects of language-specific linguistic environment on perceptual aspects of language processing. Independent of the social
interaction aspect of the linguistic environment previously discussed, culture-specific differences in formal properties of language, such as phonology and orthography, also affect language
processing. For instance, the attunement model of early experience
on phonological development suggests that culture-specific language effects could shape and trim infants’ phonetic discrimination abilities (Aslin, 1981). Young infants (5–17 weeks old) are
better at discriminating and categorizing phonetic contrasts used in
different natural languages than adults (e.g., Trehub, 1976). On the
one hand, limiting exposure during early development to the set of
phonetic categories of their own native language helps infants
maintain discrimination sensitivity to phonetic contrasts in the
native language, but on the other hand, it leads to loss of sensitivity
in discriminating sound categories of foreign languages. Thus,
adults often have difficulty discriminating nonnative phonetic contrast (e.g., Miyawaki et al., 1975; Trehub, 1976).
More recent findings comparing different language groups lend
further support. A study by Kuhl, Williams, Lacerda, Stevens, and
Lindblom (1992) shows that by 6 months of age, infants start to
discriminate reliably among sound patterns associated with the
language spoken around them but not between the sound patterns
of unfamiliar languages. Specifically, when American and Swedish infants were tested with vowel prototypes of their native
languages, the infants showed better generalizations to phonetic
variants around the prototypes contained in their native languages
(called the perceptual magnet effect). Another study comparing
two closely related languages also shows that language-specific
phoneme representation is established in infancy and maintained
throughout adult life (Näätänen et al., 1997). Finns and Estonians
speak closely related languages with very similar vowel structures,
except that the Estonians have one additional vowel /õ/ which is
roughly in between the Finnish /o/ (as in sore) and /ö/ (as in sir).
Both perceptual and neurophysiological data showed that Finnish
and Estonian adults judged the vowels common to both languages
similarly; however, the response for the /õ/ category was only
found in the Estonians (Näätänen et al., 1997). Furthermore, it was
found that these language-specific representations emerged before
the age of 12 months (Cheour et al., 1998).
In addition to language-specific phoneme effects, there is also
evidence of culture-specific language influences operating at the
level of orthographical mappings between graphemes and phonemes. In comparison to the Italian language, English orthography
is rather inconsistent, with complicated mappings of letters to
sounds. In the English language there are 1,120 ways of representing 40 sounds (phonemes), whereas in the Italian language 33
graphemes are sufficient to represent 25 phonemes. At the
cognitive–perceptual level, this culture-specific language difference leads to faster word and nonword reading in Italian university
students than in English university students (Paulesu et al., 2000).
It is also related to Paulesu et al.’s (2001) finding that the prevalence rate of dyslexia is about 50% less among Italian than among
English individuals and that, on average, Italian individuals with
LI
dyslexia show better reading performance than English individuals
with dyslexia.
Effects of language-specific linguistic environment on language
processing captured by neuronal plasticity. Culture-specific language differences do not affect language processing at the perceptual and cognitive levels only. Recent findings indicate a dynamic
shift in cortical organization over the course of language acquisition (see Neville et al., 1998, for a review). For instance, the time
course of the changes and the degree of experience-dependent
changes vary with different aspects of language. ERP data indicate
that at 20 months, when children are typically speaking in singleword utterances, open-class words (i.e., words conveying referential meaning) and closed-class words (i.e., words providing structural and grammatical information) elicit similar patterns of brain
activity (Neville & Mills, 1997). At 28 to 30 months of age, when
children typically begin to speak in short phrases, ERPs to openand closed-class words reveal different patterns of brain activity,
and by 3 years of age, when most children speak in sentences and
use closed-class words appropriately like adults, ERPs start to
display a left hemisphere asymmetry similar to adults (Neville &
Mills, 1997). In a related vein, neuroimaging data indicate strong
left hemisphere activation for the native language in bilinguals.
Whereas early bilinguals (i.e., learned their second language before 7 years of age) showed overlapping areas of cortical activation
for the native and second languages (Kim, Relkin, Lee, & Hirsch,
1997; Weber-Fox & Neville, 1996), late bilinguals showed independent or less overlapping activation (see Neville & Bavelier,
1998; Neville et al., 1998, for reviews).
Although language processing depends on a system of neural
networks primarily in the left hemisphere, within the common
system, there is room for the progressive developmental history of
learning and using languages that differ in their orthographical
mapping complexity to leave its trace at the cortical level. Italian
readers showed greater activation in the left superior temporal
regions, areas associated with phoneme processing, whereas readers of English showed greater activations—particularly for nonwords—in the left posterior inferior temporal gyrus and anterior
frontal gyrus, areas associated with word retrieval during both
reading and naming tasks (Paulesu et al., 2000). The data seem to
suggest that acquiring the rather complex orthographical mapping
of the English language impels its readers to invoke additional
neurocognitive mechanisms involving word retrieval from semantic memory while reading.
Taken together, examples from language research presented in
this section show that, at a broad level, realizations of the interconnectedness across levels and time scales unify coconstructive
conceptions, interactive processes, and developmental plasticity at
different levels into one general common frame. Viewed through
the cross-level dynamic biocultural coconstructive framework, it
becomes explicitly clear that culture–situation, culture–individual,
situation–individual, individual–situation, and situation– culture–
gene interactions jointly played out across the phylogenetic, ontogenetic, and microgenetic time scales are all central to the coevolution of language, social dynamics, and brain. While each set of
these processes is responsible for separate interactions between
specific levels, as a whole they are closely interconnected; hence,
conceptualizations of various ranges and series of cultural and
experiential effects on neurobiological processes become more
operant and more easily reified. At a more specific level, in
keeping with the examples of language research, such realizations
BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
provide insights for future investigations of social linguistic influences—such as of sociocultural influences on the development of
self-concept and autobiographical memory or of language-specific
effects mediated through parental speech on semantic development—at the neurobiological level.
Current research efforts on most other aspects of cognitive and
behavioral development are still very limited with respect to the
levels and time scales they cover. Nonetheless, converging evidence from studies of language summarized here offers promising
prospects for connecting developmental phenomena at various
levels. Such integration can be achieved by actively incorporating
considerations of different facets of cultural influences and interconnections between interactive processes across different levels
unfolding on different time scales into the day-to-day practice of
developmental research. Next, a few new insights into potential
interfaces, empirical questions, designs, and methods that would
be helpful for integrating cultural and experiential influences with
behavioral genetics and cognitive neuroscience research are
discussed.
Insights for Integrating Reciprocal Cultural and
Cumulative Developmental Influences Into Behavioral
Genetics and Cognitive Neuroscience Research
Overarching dynamic biocultural coconstructive conceptions
explicitly detailing the interconnections between interactive processes across levels of the kind proposed here are useful in guiding
more integrated research efforts across different branches of developmental and life sciences. This is a difficult challenge, yet the
evidence of reemerging coconstructive views and empirical research at all levels (see Appendix) indicates that, at least, the
possibilities are emerging. Guided by the framework, I discuss in
this last section a few new insights into potential interfaces for
reciprocal cultural and cumulative life span developmental influences to be integrated into existing behavioral genetics and cognitive neuroscience research paradigms.
Considering Cultural and Cumulative Developmental
Influences on Genetic Expressions
Regarding behavioral genetics research, a principle clearly suggested by the dynamic biocultural coconstructivism is that genetic
and environmental– cultural influences interact cumulatively with
each other across the life span, jointly affecting behavioral and
cognitive development. At first glance, this seems a trivial point.
Yet, thus far the traditional “additive model” of behavioral genetics research has treated nature and nurture orthogonally, as if these
two sources of influence added up to 100% of the variance in a
given behavioral or cognitive characteristic. Only recently have
influences on genetic effects by experiential and cultural interactions across the life span been emphasized (Baltes, 1997; Dick &
Rose, 2002; R. J. Rose, 1995) and new research paradigms started
to emerge. For instance, with respect to cultural and experiential
influences mediated through the proximal developmental context,
Collins et al. (2000) pointed out that traditional behavioral genetic
research on genetic and parenting effects could be augmented with
designs affording either experimental comparisons of differing
parental factors on individuals with varying biological influences
or controls of biological factors. New statistical models have also
been recently developed to model reciprocal causation between
185
phenotypic behavioral and cognitive expressions and the proximal
developmental context (Dickens & Flynn, 2001).
Cohort design as a window into history-graded cultural influences on genetic heredity. It is conceivable that similar principles
could be generalized to examine the interactions between genetic
influences and other culture-specific influences in individuals’
proximal developmental contexts. For example, in within-culture
contexts, birth cohort effects are not just influences that need to be
controlled for in longitudinal studies. In fact, they may represent
history-graded cultural changes that are primarily driven by technological developments and changes in population factors, such as
overall socioeconomic levels. In this vein, studies combining longitudinal cohort-sequential or cross-sequential designs (e.g.,
Baltes, 1968; Schaie, 1965) with the emphases of behavioral
genetics research could open up possibilities for exploring questions on how heredity coefficients might also be influenced by
environmental and cultural factors operating within the proximal
developmental contexts of different cohorts.
Recent findings from a population-based Danish twin study
(Kohler, Rodgers, & Christensen, 1999) suggest that considerations of demographic regimes shifting the relative magnitudes of
genetic and environmental– cultural contributions to behavior and
cognition may not be as irrelevant as they might seem. The authors
compared twins born during 1879 –1910 and 1953–1964. Although genetic influences on fertility existed (estimated to be
about 30%–50% in this sample), the relative patterns were contingent on gender and, of particular interest here, on the socioeconomic environment experienced by the two cohorts. As genetic
dispositions may primarily affect fertility behavior and motivations for having children, the effect of genetic influence on fertility
was accentuated in the later cohort, in which individuals had more
deliberate control over fertility and for which the relatively egalitarian socioeconomic opportunities weakened environmental influence across individuals.
Life span research as a window into cumulative developmental
influences on genetic heredity. It is also important to consider the
effects of development and aging on the relative balance between
nature and nurture (Baltes, 1997; Plomin & Crabbe, 2000). For
instance, at the descriptive level, heritability of general cognitive
ability measured by intelligence tests changes across the life span.
Estimates of heritability are about 20% in infancy, 40% in childhood, 50% in adolescence, and 60% in adulthood and in individuals aged 80 years and older (e.g., McClearn et al., 1997; McGue,
Bouchard, Iacono, & Lykken, 1993). In addition to cognitive
abilities, among twins the extent of genetic influences on physical
functional abilities in old age was also found to be larger among
individuals aged 80 years and older than among individuals
aged 75 to 79 years (Christensen et al., 2000). It is interesting that
concomitant with the increased genetic influences on physical
functional ability in the fourth age (i.e., aged 80 years and older)
is a significant share of environmental influence on older adults’
health control beliefs, shifting the locus of control from endogenous self-pertaining factors to exogenous social contextual factors,
such as the influence and support from powerful others (Johansson
et al., 2001). Taken together, these findings motivate further explorations of the causes and processes, including self-regulatory
mechanisms such as motivation and control beliefs, that may
underlie developmental and aging effects on the relative contributions of genetic and environmental influences on cognitive abilities
and physical bodily functions in different periods of the life span.
186
Considering Cultural and Cumulative Developmental
Influences on Cognitive Style and Cortical Functioning
Regarding cognitive neuroscience research, there are many possible interfaces for designing research paradigms to more directly
study the cultural and cumulative life span developmental influences on cognitive style and learning- and experience-dependent
cortical plasticity. In dealing with developmental disorders,
Karmiloff-Smith and associates have already argued for the importance of considering the possibility of multiple bidirectional
mappings from biology to cognition to behavior. Specifically, it
has been suggested that apparent normal behaviors may be
achieved by different processes at the cognitive level, which may
in turn be implemented differently at the neurobiological level.
This could be most evident in the case of neurodevelopmental
disorders because the cognitive–neuronal system has had to work
around its deficits during development as much as possible (see
Karmiloff-Smith, 1998, for a comprehensive review).
Neurocognitive aging as a window into cultural and cumulative
developmental influences on neuronal processes. Neuroimaging
data on age-related reduction in lateralization of cognitive information processing (e.g., Cabeza, 2002; Cabeza et al., 1997;
Reuter-Lorenz, 2002; Reuter-Lorenz et al., 2000) hint at an analogous picture on cognitive aging. It seems that in response to
aging-related decline in brain efficacy and integrity, “apparent
nominal cognitive tasks” (i.e., tasks with seemingly identical requirements) are implemented differently in the aging brain. It
remains to be seen how much of the cortical functional change
reflects neuronal compensatory functional plasticity in the face of
losing structural and/or neurochemical integrity; how much reflects the decline in structural, functional, and/or neurochemical
integrity itself (e.g., Logan, Sanders, Snyder, Morris, & Buckner,
2002); and how much is due to changes in processing strategies at
the cognitive and behavioral levels. Answers to these questions
may not be straightforward, however, because these different aspects are not independent of each other. Neurocomputational models could be useful tools for theoretical investigations of these
intertwined relations (e.g., S.-C. Li et al., 2001; S.-C. Li & Sikström, 2002).
Neurocognitive aging as a window into cultural and cumulative
developmental influences on cognitive style and expertise acquisition. In a related vein, recent reports of cultural influences on
cognitive styles showing that East Asians process information in a
more holistic and contextualized manner whereas Westerners process information in a more analytic and feature-based style (Choi
et al., 1999; Nisbett, Peng, Choi, & Norenzayan, 2001; Norenzayan & Nisbett, 2000) suggest that similar cognitive tasks may be
processed rather differently by individuals in different cultural
contexts. Research on how cultural differences might influence the
relationship between aging and cognition has already begun (Park,
Nisbett, & Hedden, 1999). Juxtaposing the results from cognitive
neuroscience studies on aging and cortical functional lateralization
with the cognitive– behavioral research on cultural influences on
cognitive style and aging, it seems a possible prospect to integrate
designs with both culture-sensitive and culture-invariant cognitive
tasks in the cognitive neuroscience approach to examine how
environmental and cultural influences interact with the aging processes at the behavioral, cognitive, and neurobiological levels.
A further possibility for examining cultural influences on cognition and experience-dependent neuronal plasticity seems to lie in
LI
the interface between the behavioral experimental and cognitive
neuroscience approaches to aging, expertise, and training research.
Take language expertise as an example: comparing the performance of young and old early and late bilinguals (i.e., individuals
who started learning the second language either before and after
the age of 7 years, respectively) may help understand the interactions among the age of acquisition, aging effects on expertise in
language processing, and the related neuronal processes. There
have been very few studies comparing young and old bilinguals,
and the results show age-related declines in language expertise,
particularly in conditions involving switching between two languages (Hernandez & Kohnert, 1999). In addition, there seems to
be a similar decline in both languages, suggesting nonmodular
aging effects on first and second language skills (Juncosrabadan,
1994). Given the evidence showing that only early bilinguals
exhibit overlapping cortical activation for first and second languages (Neville & Bavelier, 1998), it remains to be seen whether
modular (vs. nonmodular) aging effects on language expertise are
related to an individual’s age at second-language acquisition and
the extent of overlapping cortical processing between the
languages.
In addition to empirical investigations, neurocomputational
models, with their dynamic adaptive properties depending both on
the input– output mapping contexts and training history, lend
themselves as suitable tools for studying environmental support
(Craik & Anderson, 1999) and experiential and progressive developmental influences on different aspects of cognitive development
and aging. For instance, there are examples of neural network
models capturing developmental specifications of language (e.g.,
Elman et al., 1996; Guenther & Gjaja, 1996) and face processing
(e.g., de Haan, Humphreys, & Johnson, 2002; de Haan, Pascalis, &
Johnson, 2002) in children. Regarding aging, recent neurocomputational theories have been developed to capture the relations
between aging-related decline in neuromodulation and the dedifferentiation (or despecification) of cognitive abilities and other
aspects of cognitive processing (e.g., S.-C. Li et al., 2001), attentional control regulation (e.g., Braver et al., 2001), and error
processing (Nieuwenhuis et al., 2002) during aging.
Considering Cultural and Cumulative Developmental
Influences on Neurodevelopmental Disorders
In addition to studies on normative functioning, cultural factors
may also be implicated in the behavioral, cognitive, and neuronal
aspects of pathological deficits (Fabrega, 1977; Kennepohl, 1999).
Consider the possibility of examining cultural influences on component processes subserving the development of the ability to
predict other individuals’ intentions and behavior (i.e., theory of
mind), such as attributing desires, engaging in shared attention,
and monitoring eye gaze. Although some of these components
seem to be related to certain neurobiological substrates and to
selective impairment in social– cognitive function in individuals
with neurodevelopmental disorders such as autism (see BaronCohen, 1995; Frith & Frith, 1999, for reviews), the question as to
whether the development of these processes could be influenced
significantly by cultural factors is still open. It is not likely that the
functions and developmental sequences of these processes in general would vary much across different cultures. However, crosscultural variations in whether individual control is considered to be
internal or external, interpersonal dependent or independent, and in
BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
how necessary it is to explain the internal states of other individuals are all possible sources of cultural influences on the development of theory of mind (Lillard, 1998). Taking a more domainrelevant (Karmiloff-Smith, 1998) rather than domain-specific
view, it is not implausible that clear cultural differences in culturally embedded parental styles (e.g., emphasizing interpersonal vs.
object orientation, interdependent vs. independent self-concept)
may interact with the developmental details of these functions,
which then would need to be considered when applying clinical
assessment instruments and test batteries across countries.
I now consider the example of another neurodevelopmental
disorder, Williams syndrome (involving the microdeletion on the
long arm of chromosome 7 at q11.23), in it has been shown that
there is a within-syndrome double dissociation in terms of uneven
phenotypic cognitive profiles expressed in infancy and adulthood.
Whereas the ability for numerosity judgment is spared in infancy
but impaired in adulthood, language ability is impaired in infancy
but spared in adulthood (Paterson, Brown, Gsödl, Johnson, &
Karmiloff-Smith, 1999). This indicates the importance of including progressive developmental influences into behavioral genetics
and cognitive neuroscience research on developmental disorder.
With respect to Williams syndrome, one can also think of analogous implications with respect to including cultural influences into
the research designs. For instance, the uneven phenotypic cognitive profiles of spared verbal fluency and relatively impaired
spatial-constructive and spatial-perceptual skills in adulthood
might interact with the differing phonological and orthographic
emphases and syntactic and lexical constraints in different languages, thereby affecting the hemispheric lateralization of language processing. To illustrate, the Japanese language has two
systems of signs, the ideograms of Kanji characters and the phonetic Kana signs. The left hemisphere is mostly involved in the
processing of the phonetic Kana signs, similar to other phonetic
languages used in Western cultures. Damage to either the Broca’s
or Wernicke’s area has clear impact on the use of Kana. The right
hemisphere is more involved in processing the Kanji ideograms
(Elman, Takahashi, & Tohsaku, 1981; Sasanuma, 1975). A case
study showing that a 9-year-old Japanese boy with Williams
syndrome had difficulty writing the visual-based Kanji ideograms,
which he could otherwise read and understand (M. Nakamura et
al., 1999), implies that culture-specific language differences might
interact with the processes involved in neurodevelopmental
disorders.
Conclusion
Genomics research is dashing ahead to unfold the map of the
complete human genome, but the genome sequence on its own will
never be able to construct a human being out of the human
organism. Neural imaging and other newly advanced techniques of
neuroscience are now getting at the details of how the brain
operates at various levels to give rise to different aspects of mental
phenomena— even how the brain operates to give rise to consciousness and to one’s sense of self and others. However, the
questions of what contents the brain generates and of how the very
contents the brain generates and operates on may exert reciprocal
influences on its structure and function cannot be answered if the
contexts of neural information processing, brain development, and
biological evolution are not considered. Evidence reviewed in this
article indicates that reduction without contexts (i.e., without the
187
cultural, experiential, and cumulative developmental contexts)
alone would not help us understand the neurobiological bases of
mind and behavior. The reason is clear: Genetic activities and
neuronal mechanisms themselves possess remarkable plasticity
awaiting environment and culture to exert selective developmentand experience-based reciprocal influences (cf. Edelman, 1987) on
them and to be the “coauthors” of mind and behavior. People are
more than mere biological organisms; human mind and behavior
need to be understood by situating them properly within a brain in
a body that lives in an eventful world abounding with objects and
people. Indeed, the brain offers the necessary biophysical reality
for individual cognition and action; it alone, however, is not
sufficient to engender the mind or behavior. On the mind– brain
continuum, the individual mind is the expression emerging from
the personalized brain (Greenfield, 2000; Llinas & Churchland,
1996). The very processes for personalizing the biological faculty
of the mind take place throughout life span development in environmental and sociocultural contexts, which entail intimate dynamical exchanges between nature and nurture.
This review shows that there is accumulating evidence for
developmental plasticity at different levels of analyses that reflect
and implement, together with closely connected interactive processes across levels, bidirectional reciprocal biocultural influences
throughout the life span. A cross-level dynamic biocultural coconstructive framework suggests new insights of possible interfaces
for the reciprocal cultural influences to be considered and integrated into current behavioral genetics and cognitive neuroscience
research. The task of understanding how individual brains get
personalized throughout life span development to engender individual minds as individuals live together with other sapiens colleagues in a social world abounding with cultural historical heritage calls for a new stage of transdisciplinary collaboration
involving biocultural life span developmental sciences.
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BIOLOGY AND CULTURE IN DEVELOPMENTAL PLASTICITY
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Appendix
Coconstructive Conceptions and Evidence of Developmental Plasticity at Different Levels
Theoretical notions
Empirical evidence of plasticity
Coevolution of genes, cognition, and culture
(Dunbar, 1993, 1998; Donald, 1991; Durham,
1991; Edelman, 1992; Hutchins, 1995)
Interactive and coactive evolutionary
framework between biology, cognition, and
culture
Niche construction
(Laland et al., 2000)
The activities, choices, and metabolic
processes through which organisms define,
choose, modify, and create their living
environment to further modify selection
pressures by feedback to biological
evolution or cultural changes
Development and behavior initiated evolutionary
change
(Gottlieb, 2002)
Behavioral changes incurred during
development instigate genetic changes if
transgenerational environmental rearing
conditions are relatively stable.
Cultural and evolutionary plasticity: receptivity of culture to
modifications by individual behaviors and new technology and
the susceptibility of biological evolution to cognitive and cultural
influences
Learning and experience influence the adoption of culture traits
(Durham, 1991).
Automation and electronically distributed knowledge
representation and computer-coordinated planning affect the
relative roles of individual minds and external memory devices
(e.g., Hutchins, 1995).
Invention of writing leads to other inventions (e.g., printing,
electronic mail; Laland et al., 2000).
Relative neocortical volume in nonhuman primates is related to
social group size (Dunbar, 1993, 1998).
Diary farming selects for lactose tolerance (Aoki, 1986; Feldman
& Cavalli-Sforza, 1989).
Incipient specification mediated by developmental–behavioral
changes in the apple maggot fly (this and other examples are
reviewed in Gottlieb, 2002).
Evolutionary biology
and psychology
Developmental phenomena need to be studied by
considering interactional influences at various
levels. The following conceptualizations share the
general notion that individual development is
hierarchically organized into multiple levels in an
open developmental system:
Social-contextual influences
(Vygotsky, 1978)
Bioecological model
(Bronfenbrenner & Ceci, 1994)
Interactional and holistic framework
(Magnusson, 1988, 1996)
Cultural-social contextual framework
(Cole, 1999; Cole & Cole, 1989; Gauvain, 1995)
Biocultural linguistic experiential framework
(Nelson, 1996; Nelson, Plesa & Henseler, 1998)
Relationship contextual approach
(Reis et al., 2000)
Interpersonal neurobiology approach
(Siegel, 1999)
Evolutionary developmental psychology
(Bjorklund & Pellegrini, 2000, 2002; Geary &
Bjorklund, 2000)
Dynamic system approach
(Smith & Thelen, 1993; Thelen & Smith, 1994;
van Geert, 2000)
Behavioral and cognitive plasticity: socialization and learningdependent cognitive and behavioral development across the life
span
The quality of proximal parental style (e.g., mother–infant
interaction) at early ages (2–4 years) affects the amount of
problem behavior later in life (Bronfenbrenner & Ceci, 1994;
Drillien, 1964).
The degree of proximal parental monitoring affects school
achievement in adolescence (Bronfenbrenner & Ceci, 1994).
Neighborhood context affects parental style, which subsequently
affects social development in children (Furstenberg, Eccles,
Elder, Cook, & Sameroff, 1997).
Differences in emphasizing interpersonal versus object orientation
in 5-month-old babies in Japan and the United States affect the
types of languages and playing toddlers are good at (Bornstein
et al., 1991).
Culture affects individuals’ style of causal attribution (Choi et al.,
1999; Norenzayan & Nisbett, 2000).
Cultural influences on the style of parental speech affect language
development and autobiographical memory (e.g., Gopnik et al.,
1996; Mullen, 1994; Wang et al., 2000).
At 6 months of age, infants can discriminate sound patterns of
their own languages (Kuhl et al., 1992).
Language-specific memory traces develop in infants at the age
of 12 months and are maintained throughout adult life (Cheour
et al., 1998; Näätänen et al., 1997).
Developmental
psychology
Hebbian rule and long-term potentiation (LTP)
(Bliss & Lømo, 1973; Hebb, 1949)
Convergence of firing activities among
repeatedly and simultaneously active
neurons leads to activity-dependent
strengthening of synaptic connections.
Epigenesis by selective stabilization
(Changeux, 1985; Changeux & Danchin, 1976)
Although genes regulate the division,
migration, and differentiation of nerve cells,
epigenetic interactions affect phenotype
variations in fine details of cortical
organization.
Neuronal plasticity: behavior- and experience-dependent
synaptogenesis, neurogenesis, and functional plasticity
LTP is important in associative learning and memory. For
instance, enduring LTP is observed in hippocampal networks
during encoding of associative information (see Squire &
Kandel, 1999, for review).
Rats reared in enriched environments showed more mature
synaptic structure, more dendritic spines, more synapses per
neuron, better blood supply, more protein content, increased
level of neurotransmitters, and growth of new neurons (e.g.,
Black & Greenough, 1998; Greenough & Black, 1992; Gross,
2000; Rosenzweig, 1996).
Cognitive neuroscience
and neurobiology
(Appendix continues)
Levels/fields
LI
194
Appendix (continued)
Theoretical notions
Empirical evidence of plasticity
Levels/fields
Neuronal group selection theory
(Edelman, 1987; Edelman & Mountcastle, 1978)
Although the anatomical structure of the brain
is constrained in part by genetic inheritance,
cortical organization of cognitive function
arises from parallel reciprocal connections
between neuronal groups that are
established by developmental and
experiential selection taking place
throughout life.
Experience-dependent synaptogenesis
(e.g., Greenough & Black, 1992)
Experience-dependent development of synaptic
connections
Cortical functional plasticity
(Hamilton & Pascual-Leone, 1998, for a review)
Experience-dependent and compensatory
changes in functional circuits (e.g., synaptic
connectivity, functional localization) in
various brain regions
Epigenetic interactions affected the patterns of axonal branching
in genetically identical clonal water fleas (Changeux, 1985;
Levinthal, Macagno & Levinthal, 1976).
Although genetic factors have substantial influences on human
cerebral size (e.g., Pennington et al., 2000), the overall cortical
gyral patterns, though also affected by genes, are affected by
nongenetic factors (Bartley et al., 1997).
Enlarged sensorimotor representation of blind individuals’ Braillereading fingers (see Hamilton & Pascual-Leone, 1998, for a
review).
Reorganization of cortical sensory representation in terms of
compensatory plasticity; for instance, binocularly deprived cats
showed improved auditory localization ability (see Rauschecker,
1995, for a review).
Cortical representation of the left fingers of stingplayers was
larger than that of the right fingers (Elbert et al., 1995).
The size of posterior hippocampi was enlarged in individuals
relying heavily on their navigation skills in daily activities
(Maguire et al., 2000).
Dynamic shift in cerebral organization has been found as infants
start to learn their native language (Neville et al., 1998).
Probabilistic epigenesis
(Gottlieb, 1991, 1998, 2000)
The production of a functional organism
requires a system with bidirectional genetic,
neural, behavioral, and environmental
influences.
Genetic plasticity: environment and experience-dependent
genetic activity and expressions
In songbirds, species’ songs stimulate the activation of a set of
genes in the forebrain to further regulate the expression of other
genes in the same region (Mello et al., 1992).
In rats, a behavioral learning task involving the vestibular system
affected the base nuclear RNA ratios in the vestibular system
(Hydèn & Egyhàzi, 1962).
In rats, visual stimulation affected RNA and protein synthesis
(particularly RNA diversity) in the visual cortex (Grouse,
Schrier, Letendre, & Nelson, 1980; S. P. R. Rose, 1967).
In humans, psychological stress affects mRNA activities regarding
the immune system (Glaser et al., 1990).
Maternal style affects gene expression in reaction to stressors in
Rhesus monkeys (Suomi, 1999).
In humans, social stressors affect concentration of lymphocyte
growth hormone (L-GH) in late adulthood. Caregivers of
spouses with Alzheimer’s disease showed markedly suppressed
L-GH concentration (Malarkey et al., 1996).
Behavioral genetics and
biogenetics
Received April 19, 2001
Revision received June 21, 2002
Accepted June 24, 2002 䡲