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Oxford Handbook of Developmental Behavioral Neuroscience OXFORD LIBRARY OF NEUROSCIENCE Editor-in-Chief GORDON M. SHEPHERD Oxford Handbook of Developmental Behavioral Neuroscience Edited by Mark S. Blumberg John H. Freeman Scott R. Robinson 3 2010 Introduction: A New Frontier for Developmental Behavioral Neuroscience Mark S. Blumberg, John H. Freeman, and Scott R. Robinson As editors of this volume, we wrestled with alter- (2) to highlight current opportunities to advance native titles to capture what we felt was a theo- our understanding of behavioral and neural devel- retically connected but highly interdisciplinary opment through enhanced interactions between fi eld of science. Previous edited volumes that have DP and its sister disciplines. addressed related content areas were published In 1975, in his infl uential book Sociobiology: over a 15-year span beginning in the mid-1980s T e New Synthesis, E. O. Wilson famously looked under the label of “developmental psychobiology” forward to the year 2000 when, he predicted, (e.g., Blass, 1986, 1988, 2001; Krasnegor, Blass, the various subdisciplines of behavioral biology Hofer, & Smotherman, 1987; Shair, Hofer, & Barr, could be represented by a fi gure in the shape of a 1991). Although all three of the editors of the pre- barbell—the narrow shaft representing the dwin- sent volume have longstanding ties to the fi eld of dling domain of the whole organism (i.e., ethology developmental psychobiology (DP) and its parent and comparative psychology) and the two bulging society (the International Society for Developmental orbs at each end comprising the burgeoning fi elds Psychobiology), we also view our work as part of a of sociobiology and neurophysiology. Wilson’s pre- larger community of researchers in behavioral neu- diction that the study of the whole organism would roscience, comparative psychology, developmental be “cannibalized” by population and reductionistic science, and evolutionary biology. T is volume is approaches seemed, to many behavioral research- aimed at this larger research community concerned ers over the last quarter century, to be relentlessly with empirical and theoretical issues about behav- fulfi lled. But ultimately, the “death of the organ- ioral and neural development. ism” has proven greatly exaggerated. On the con- DP has traditionally concerned itself with inves- trary, we are witnessing a resurgence of interest in a tigations of the biological bases of behavior and how diversity of mechanisms—especially developmen- they change during development. T e rich tradition tal mechanisms—that contribute to the form and of DP is seen in the many advances it has provided function of the organism. Most importantly (for to our understanding of behavior and behavioral this volume), the behavior of whole organisms has development. Moreover, DP has been distinguished emerged as a central product and causal infl uence by its adherence to an epigenetic perspective, that of developmental change. is, a perspective that embraces all contributions to Wilson’s view of the future from his 1975 individual development, from the molecular to the perch refl ected two biological themes–cell theory social. DP remains a productive and innovative dis- and evolutionary theory–that were central to the cipline, but it now faces new challenges posed by rise of modern biology in the nineteenth century rapid advances and the advent of powerful technol- and which were greatly refi ned and expanded in ogies in molecular biology, neuroscience, and evo- their infl uence in the twentieth century. By the lutionary biology. T ese challenges, however, are mid-twentieth century, these two perspectives cul- also opportunities. T us, our goal for this volume minated in the rise of the Modern Synthesis, the is twofold: (1) to communicate the central research discovery of DNA, and the success of the molecu- perspectives of DP to a wider community inter- lar revolution. T e new emphasis on parts and pop- ested in behavioral and neural development and ulations anchored Wilson’s barbell and relegated the organism to a transient vessel, a mere convey- (1967) at least called attention to the value of devel- ance for selfi sh genes (Dawkins, 1977). On the one opmental analyses of behavior and expanded the hand, the Modern Synthesis succeeded in reconcil- traditional dichotomy of causes into four “causes ing Darwinian evolution with population genetics and origins” of behavior: (1) causation or control (Provine, 1971); on the other, the successes of molec- (immediate physiological mechanisms), (2) devel- ular biology convinced many that whole organisms opment (history of change in the individual), could be reduced to individual traits and crucial (3) adaptive signifi cance (mechanisms acting on biochemicals produced through the actions of sin- past populations, such as natural selection), and gle genes (Keller, 2000; Moore, 2001). Although (4) evolution (history of change in the population). many prominent scientists tried very hard to off er But whether viewed as two, four, or even more clas- plausible alternatives and amendments to these two ses of cause, such classifi cation schemes have reifi ed dominant perspectives (Alberch, 1982; Gottlieb, the notion that biological causes can be treated as 1992; Gould & Lewontin, 1979; Lehrman, 1953; distinct and independent entities. Stent, 1977), they were unable to stem the tide. Tinbergen’s four-question scheme has been Proximate causes are the immediate conditions widely adopted in textbooks and behavioral train- that give rise to behavior. Such causes include ing programs and has contributed a great deal to the activity in particular neural circuits, the actions of clearer formulation of research questions in ethol- neuro transmitters at specifi c receptors, the modulat- ogy and comparative psychology (Dewsbury, 1994; ing infl uence of hormone molecules, and the trans- Hailman, 1982; Hogan, 1994; Sherman, 1988). duction of sensory stimuli into neural responses. But it also has obscured deep underlying connec- In contrast, ultimate causes refer to the function or tions between these areas of inquiry. For instance, purpose of behavior, which in evolutionary terms we are coming to appreciate that—in contrast to is the result of natural selection acting on popula- the comparative anatomy of behavior espoused tions. Although the distinction between proximate by Lorenz (1937, 1981)—behavior is not an entity and ultimate causation is evident in the early writ- such as a bone or internal organ that has a continu- ings of both biologists (Baker, 1938; Huxley, 1916; ous existence. Rather, each behavioral performance Lack, 1954) and comparative psychologists (Craig, is unique and ephemeral, although it may be recog- 1918; Dewsbury, 1999), this dichotomy of causes nizably similar to other performances by the same was promoted most eff ectively by Ernst Mayr individual in the past or other individuals of the (Beatty, 1994; Mayr, 1961), a central fi gure in the same species. Behavior is elaborated in time despite rise of the Modern Synthesis. Interestingly, Mayr the common research practice of treating individ- used proximate and ultimate causation as indepen- ual behavioral acts as instantaneous for purposes dent explanations to defend evolutionary interpre- of analysis. From these perspectives, the causation tations from criticisms coming from mechanistic of behavior, which encompasses the “proximate” physiologists and molecular biologists (Amundson, physiological mechanisms that generate behavior, 2005; Dewsbury, 1999; Mayr, 1974). In eff ect, also should be seen as a question of historical ori- Mayr appealed to the explanatory categories of gins, albeit on a much briefer time scale and there- proximate and ultimate causation to delineate the fore within the same continuum of phenomena as fi elds of molecular–cellular and population biol- development. ogy, thereby creating the very barbell that Wilson T eorists since Darwin also have recognized par- conveniently “predicted” in 1975. allels in patterns of change on developmental and Of course, what was missing from both the evolutionary time scales. Early attempts to explain Modern Synthesis and the reductionism of molec- the phylogenetic information evident in embryolog- ular biology was an adequate appreciation for the ical development were founded on notions such as role of development as a mediating cause of organic Haeckel’s biogenetic law, which stated that embryos change. As long as genes were viewed as root causes pass through the same sequence of stages during of individual characteristics (necessary for a mod- development as the adult forms of ancestral species ern synthetic interpretation of evolution), and gene during evolution (Haeckel, 1866). Although strong frequencies in populations were viewed as suffi cient forms of recapitulation have long since been discred- metrics of evolution, it was possible to skip over the ited (Gould, 1977), developmental issues have risen messy details of how a fertilized egg is transformed in prominence again over the last several decades into an organism that can, in turn, be a target of within both the evolutionary (Kirschner & Gerhart, natural selection. Tinbergen (1963) and Hailman 2005; West-Eberhard, 2003) and molecular (Carroll, INTRODUCTION: A NEW FRONTIER FOR DEVELOPMENTAL BEHAVIORAL NEUROSCIENCE 2005) domains. Moreover, the success of unsuper- 2005, 2009; Gottlieb, 1997; Oyama, Griffi ths, & vised processes such as natural selection in explain- Gray, 2001; West, King, & Arberg, 1988). Although ing evolutionary change has led to similar
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