The Emergence of Developmental Neuroethology Donald J. Stehouwer Departments of Psychology and Neuroscience, Center for Neurobiological Sciences and the University of Florida Brain Institute, University of Florida, Gainesville, Florida 3261 1 The dramatic progress in our understanding of the nervous system has been recognized by the U.S. Congress in its declaration of the 1990s as the Decade of the Brain. Much of that progress has resulted from technical developments that enabled the emergence of whole new areas of inquiry. Other areas of brain research, while incorporating technical advances, owe their fertility primarily to new conceptualizations of old problems and to a fusion of existing branches of the biological sciences. Nowhere is this more evident than in the field of neuroethology, a field which traces its roots to several parental disciplines, including psychology, zoology, ethology, neurophysiology, and neuroanatomy. In neuroethology, these complementary disciplines are united in a single integrated approach to problems of understanding the brain and behavior. Like its parent, ethology, the primary focus of neuroethology is on species-specific, naturally occumng behavior, rather than on arbitrary measures ofbehavior, such as rate ofbar-pressing or the number of photocell beams broken in an activity apparatus. Unlike some areas of the neurosciences that use behavioral measures, behavior is the object of study rather than an assay used to assess the effects of different treatments thought to alter brain function. Neuroanatomy, neurophysiology,neuropharmacology, and neuroendocrinology are interesting only because of their contributions to understanding the ways in which behavior is organized, controlled, and produced. Thus, two hallmarks of neuroethology are interdisciplinary studies and vertical integration of levels of analysis, from behavior to the cell. The focus on naturally occumng behaviors, or fixed action patterns, arises from the assumption that evolution of the nervous system is driven primarily by pressures of natural selection Journal of Neurobiology, Vol. 23, No. 10, pp. 1353-1354 ( 1992) 0 1992 John Wiley & Sons, Inc. CCC 0022-3034/92/101353-02
on behavior, and that the behaviors subject to evolutionary pressure are those that are characteristic of the species under natural conditions. The neuroethological approach to the study of the nervous system function derives its strength from its ability to reveal biologically meaningful principles of organization and function. Nervous system circuits defined in terms of their participation in fixed action patterns are much more likely to reflect functional units than are circuits defined solely by anatomical or neurochemical criteria. However, because species-typical behaviors are by definition peculiar to the species under study, this approach could result in many isolated islands of information about many different systems, none which are clearly related to any other. This risk is very real, but the results of neuroethological research strikingly demonstrate that similar problems frequently have similar solutions in evolutionarily disparate species. That divergent species independently converge on similar solutions should give greater, not lesser, confidence that such solutions reveal fundamental principles of nervous system function and have general biological significance. The comparative nature of neuroethology acquires a second dimension when ontogeny is added to the equation. It has become clear in recent years that one must adopt new strategies when studying developing organisms; the tried-and-true methods developed in work on adults often simply fail to work or, worse, yield incorrect and misleading results when applied to developing organisms. Thus, much of the work of the developmental neuroethologist is devoted to identifying those conditions under which the developing organism can display its full potential. In the case of animals that undergo metamorphosis, the need for sensitivity to the peculiar demands of organisms at different stages of development is obvious. However, it has become clear that even species that do not undergo metamorphic transformation and in which ontogentic morphologicalchange is less dramatic, devel1353
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opmental studies require inventive techniques for effective study. The goal of this special issue is to introduce developmental neuroethology as a coherent, but not monolithic, approach to the study of developmental problems. Because this is, to my knowledge, the first publication devoted solely to developmental neuroethology, it is my hope that this special issue will help to define the field. Because it is a first, it seems wise to define developmental neuroethology sharply yet broadly. Some authors have taken a narrow view, arguing that there can, at present, be no such thing as vertebrate neuroethology because behavior of vertebrates cannot, at present, be understood in terms of individual neurons (Hoyle, 1984). In contrast, this special issue of the Journal qf Neurobiology defines neuroethology more broadly, and includes articles on insects (Truman), crustaceans (Govind), fish (Hagedorn, Vischer and Heiligenberg), amphibians (Stehouwer) , birds (Arnold; Bekoff), and mammals (Robinson and Smotherman; Fentress; Leon). Likewise, in tracing the roots of developmental neuroethology, the contributions both of classical ethologists (Fentress) and of embryologists (Oppenheim) are recognized. Thus, developmental neuroethology is defined here as the science devoted to explaining the ontogeny of naturally occurring behavior in terms of underlying neural mechanisms. Although the chapters seem disparate, there are
several themes that provide common threads throughout this issue. Among them are the roles that hormones play in constructing circuits for species typical behaviors (Arnold; Truman), the fate of circuits for behaviors that appear early in developnient and subsequently disappear (Bekofi Robinson and Smotherman; Stehouwer; Truman), how sequences of behavior become organized during ontogeny (Fentress; Robinson and Smotherman), the role of experience in shaping the nervous system and behavior (Arnold; Govind; Leon), communication and interactions with conspecifics(Hagedorn, Vischer and Heiligenberg;Arnold; Leon), species comparisons (Arnold; Leon), and the role of context in the expression of behavior (BekoR Fentress; Hagedorn, Vischer, and Heiligemberg; Robinson and Smotherman; Stehouwer). The attentive reader will be well rewanded with a deeper understanding of how particular species have solved specific problems of behavioral development, how nervous systems cope with changing demands during ontogeny, and with an appreciation of not only the distinctiveness,, but also of the commonality, of seemingly unrelated problems of neurobehavioral development. REFERENCE HOYLE,G. ( 1984). The scope of neuroethology. Behav. Bruin Sci. 7: 367-412.
on behavior, and that the behaviors subject to evolutionary pressure are those that are characteristic of the species under natural conditions. The neuroethological approach to the study of the nervous system function derives its strength from its ability to reveal biologically meaningful principles of organization and function. Nervous system circuits defined in terms of their participation in fixed action patterns are much more likely to reflect functional units than are circuits defined solely by anatomical or neurochemical criteria. However, because species-typical behaviors are by definition peculiar to the species under study, this approach could result in many isolated islands of information about many different systems, none which are clearly related to any other. This risk is very real, but the results of neuroethological research strikingly demonstrate that similar problems frequently have similar solutions in evolutionarily disparate species. That divergent species independently converge on similar solutions should give greater, not lesser, confidence that such solutions reveal fundamental principles of nervous system function and have general biological significance. The comparative nature of neuroethology acquires a second dimension when ontogeny is added to the equation. It has become clear in recent years that one must adopt new strategies when studying developing organisms; the tried-and-true methods developed in work on adults often simply fail to work or, worse, yield incorrect and misleading results when applied to developing organisms. Thus, much of the work of the developmental neuroethologist is devoted to identifying those conditions under which the developing organism can display its full potential. In the case of animals that undergo metamorphosis, the need for sensitivity to the peculiar demands of organisms at different stages of development is obvious. However, it has become clear that even species that do not undergo metamorphic transformation and in which ontogentic morphologicalchange is less dramatic, devel1353
1354
Stehouwer
opmental studies require inventive techniques for effective study. The goal of this special issue is to introduce developmental neuroethology as a coherent, but not monolithic, approach to the study of developmental problems. Because this is, to my knowledge, the first publication devoted solely to developmental neuroethology, it is my hope that this special issue will help to define the field. Because it is a first, it seems wise to define developmental neuroethology sharply yet broadly. Some authors have taken a narrow view, arguing that there can, at present, be no such thing as vertebrate neuroethology because behavior of vertebrates cannot, at present, be understood in terms of individual neurons (Hoyle, 1984). In contrast, this special issue of the Journal qf Neurobiology defines neuroethology more broadly, and includes articles on insects (Truman), crustaceans (Govind), fish (Hagedorn, Vischer and Heiligenberg), amphibians (Stehouwer) , birds (Arnold; Bekoff), and mammals (Robinson and Smotherman; Fentress; Leon). Likewise, in tracing the roots of developmental neuroethology, the contributions both of classical ethologists (Fentress) and of embryologists (Oppenheim) are recognized. Thus, developmental neuroethology is defined here as the science devoted to explaining the ontogeny of naturally occurring behavior in terms of underlying neural mechanisms. Although the chapters seem disparate, there are
several themes that provide common threads throughout this issue. Among them are the roles that hormones play in constructing circuits for species typical behaviors (Arnold; Truman), the fate of circuits for behaviors that appear early in developnient and subsequently disappear (Bekofi Robinson and Smotherman; Stehouwer; Truman), how sequences of behavior become organized during ontogeny (Fentress; Robinson and Smotherman), the role of experience in shaping the nervous system and behavior (Arnold; Govind; Leon), communication and interactions with conspecifics(Hagedorn, Vischer and Heiligenberg;Arnold; Leon), species comparisons (Arnold; Leon), and the role of context in the expression of behavior (BekoR Fentress; Hagedorn, Vischer, and Heiligemberg; Robinson and Smotherman; Stehouwer). The attentive reader will be well rewanded with a deeper understanding of how particular species have solved specific problems of behavioral development, how nervous systems cope with changing demands during ontogeny, and with an appreciation of not only the distinctiveness,, but also of the commonality, of seemingly unrelated problems of neurobehavioral development. REFERENCE HOYLE,G. ( 1984). The scope of neuroethology. Behav. Bruin Sci. 7: 367-412.
