On Evolution by Loss of Exuberancy and Phylogeny

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On Evolution by Loss of Exuberancy and Phylogeny THE BEHAVIORAL AND BRAIN SCIENCES (1984) 7, 321-366 Printed in the United States of America Evolution and ontogeny of neural circuits Sven O. E. Ebbesson Department of Anatomy, Louisiana State University School of Medicine, Shreveport, La. 71130 Abstract: Recent studies on neural pathways in a broad spectrum of vertebrates suggest that, in addition to migration and an increase in the number of certain select neurons, a significant aspect of neural evolution is a "parcellation ' (segregation-isolation) process that involves the loss of selected connections by the new aggregates. A similar process occurs during ontogenetic development. These findings suggest that in many neuronal systems axons do not invade unknown territories during evolutionary or ontogenetic development but follow in their ancestors' paths to their ancestral targets; if the connection is later lost, it reflects the specialization of the circuitry. The pattern of interspecific variability suggests (1) that overlap of circuits is a more common feature in primitive (generalized) than in specialized brain organizations and (2) that most projections, such as the retinal, thalamotelencephalic, corticotectal, and tectal efferent ones, were bilateral in the primitive condition. Specialization of these systems in some vertebrate groups has involved the selective loss of connections, resulting in greater isolation of functions. The parcellation process may also play an important role in cell diversification. The parcellation process as described here is thought to be one of several underlying mechanisms of evolutionary and ontogenetic differentiation. Keywords: commissures; development; evolution; lateralization; learning; neocortex; neural circuits; olfactory system; ontogeny; plasticity; somatosensory pathways; superior colliculus; thalamus; visual pathways Introduction 1. What is homologous to what in various species? 2. How are new structures added on in the evolution of An understanding of the evolutionary history of brain more complex brains? structures and functions should be no less important to 3. Why do axons grow in some directions and not in the neurobiologist than the evolutionary history of galax- others during their development? ies is to the astronomer. Yet today there is no comparison 4. Why do some cells or collateral axons die during in the amount of effort in the two fields. The trend is away ontogenetic development? from studies on evolution of vertebrate brain organiza- 5. What is the significance of so-called inappropriate tion; and whereas earlier brain scientists, such as Sig- connections during ontogenesis? mund Freud and Paul Broca, were fascinated by com- 6. Why is there overlap of systems in some species and parative neurology, hardly a neurobiologist today, 100 not in others? years after Darwin, appears to think much about the 7. Why are some pathways crossed in one species and evolution of the system or process being studied. This is uncrossed in another? particularly disconcerting at a time when the comparative 8. Why are there commissural connections between data are starting to make sense, especially as they relate to some areas of cortex and not betweeen others? ontogenetic development. 9. Why does a given cortical area in one species have The fundamental problem of obtaining insights into commissural connections while the same cortical area in brain evolution is that there are no fossil records of another species lacks such connections? microscopic brain structures. Hence, we have to extract The time has not yet arrived when we can answer these information from the study of extant vertebrates. This questions completely, but hints of answers are emerging approach is now beginning to yield conceptual insights from recent data on interspecific variability of connec- into how neural systems evolve. One of these insights is tions. the recently described parcellation process, which in- volves increased neuronal migration, increase in the number of certain select neurons, and the segregation- The Nauta revolution isolation of circuits by selective loss of neurons or axonal branches. This idea and its basis are described here as an During the last few years it has become clear to some of us example of what is happening in the field, and because that an understanding of the evolution of circuits is an the idea appears to elucidate some aspects of the follow- essential requirement for understanding many aspects of ing questions confronting contemporary neurobiologists: brain structure and function and, as we shall see, normal © 1984 Cambridge University Press 0140-525X/84/030321-46/$06.00 321 Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 10:47:35, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0140525X00018501 Ebbesson: Evolution & ontogeny of neural circuits and abnormal ontogenetic development. Meaningful data about distant neural connections originated with Nauta, whose contributions have revolutionized the *aa Tb study of brain organization. His method (Nauta 1950; 1975) led not only to a vast number of new insights into X brain structure and function but also the development of a whole array of new neuronanatomical techniques for studying connectivity of the brain (Cowan et al. 1972; Fink & Heimer 1967; Kuypers et al. 1977; LaVail & c J Wd LaVail 1972). Comparative studies on nonmammalian Figure 1. The parcellation process is thought to involve the vertebrates have benefited especially from these new loss of one or more inputs to a cell, or an aggregate of cells, as research tools, and many old concepts of brain organiza- new subcircuits evolve. This diagram shows how two identical tion in such vertebrates have been replaced in the last 15 neurons (a and b) in a hypothetical aggregate become less and years (Finger 1974; Hall & Ebner 1970; Ito et al. 1980a; less influenced by a given input, with the eventual outcome that cell (a) loses input (d) and cell (b) input (c). Further parcellation Karten et al. 1973; Northcutt 1982). of such clusters can occur by some cells' losing other inputs or A major consequence of the Nauta approach was the outputs. Collaterals or the main axon may degenerate in re- discovery of well-defined interspecific differences in con- sponse to various selective pressures. The evolutionary and nections. One of the first was Mehler's (1969) finding that ontogenetic development of monocular laminae in the lateral direct spino-olivary projections are lacking in chim- geniculate nucleus and ocular dominance columns is apparently panzee and man. His findings stimulated me to engage in achieved by such a parcellation process. a long-range study of interspecific variability of connec- tions in vertebrate brains. viously believed. The data suggest that diffuse, relatively There have been two main approaches in comparative undifferentiated systems existed at the beginning of ver- neurology: to study many neural systems in one species, tebrate evolution and that during the evolution of com- as Herrick (1948) did with the tiger salamander, or to do plex behaviors and the analytical capacities related to what I have been doing, namely, approach the enormous these behaviors a range of patterns of neural systems diversity of brain organization in vertebrates by examin- evolved that subserve these functions. One principle ing a given neural system in as many different vertebrates underlying the growth, differentiation, and diversifica- as possible. I began this study with the hope that the tion of neural systems appears to be a process of "parcella- range of variation and the pattern of interspecific vari- tion" that involves the selective loss of connections in ability would provide clues about the underlying evolu- daughter systems and cellular aggregates as a result of tionary strategies. selective pressures. The result is an isolation of functions The rationale for my approach was based on several as new circuits and neuronal aggregates are formed with considerations. It was clear, for example, that one cannot connections and character different from the ancestral get an accurate picture of all systems from the study of one organization (Fig. 1-2). These concepts have recently species, since neural systems have obviously evolved at been assembled in what I have called the parcellation different rates in a given lineage. The choice of species is theory (Ebbesson 1980b; 1981). Since those publications, also not obvious, since the paleontological evidence of it has become clear that what was described as a hard rule lineages is not always clear and is difficult to relate to the probably should have been expressed as a trend and that evolution of specific neural structures and behaviors. It other variables should also be included. Hence the pre- was abundantly clear that one must look at all the arrange- sent paper. ments of a given system before one could identify and The findings in support of the theory can be listed as describe (1) the progressive and regressive evolution of follows: (1) The basic systems appear to be present in all the system, (2) the evolutionary history of a species, (3) vertebrates, and these basic systems are often more the known adaptations, and (4) the functions related to extensive in primitive species than in advanced species. the system. Neural systems apparently do not appear de novo, nor do In order to get a general picture of brain evolution, I they usually invade others
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