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Development of the Corpus Callosum and Evolution of Axon Tracts (Anterior Commissure/Axon Guidance/Glial Sling/Substrate Pathways) MICHAEL J

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Development of the Corpus Callosum and Evolution of Axon Tracts (Anterior Commissure/Axon Guidance/Glial Sling/Substrate Pathways) MICHAEL J Proc. Nati. Acad. Sci. USA Vol. 80, pp. 5936-5940, October 1983 Evolution Ontophyletics of the nervous system: Development of the corpus callosum and evolution of axon tracts (anterior commissure/axon guidance/glial sling/substrate pathways) MICHAEL J. KATz, RAYMOND J. LASEK, AND JERRY SILVER Department of Developmental Genetics and Anatomy, Case Western Reserve University, Cleveland, OH 44106 Communicated by Walle J. H. Nauta, June 13, 1983 ABSTRACT The evolution of nervous systems has included pus callosum (2, 16, 26-28). Among the placental mammals, the significant changes in the axon tracts of the central nervous sys- corpus callosum generally increases as the neocortex increases tem. These evolutionary changes required changes in axonal growth (16). The corpus callosum is a truly new feature that has ap- in embryos. During development, many axons reach their targets peared in the mammalian phylogeny during evolution (16, 28). by following guidance cues that are organized as pathways in the embryonic substrate, and the overall pattern of the major axon Ontophyletics: An embryological approach to tracts in the adult can be traced back to the fundamental pattern evolutionary questions of such substrate pathways. Embryological and comparative an- atomical studies suggest that most axon tracts, such as the anterior Special constraints operate during the evolution of those struc- commissure, have evolved by the modified use of preexisting sub- tures, such as axon tracts, that are built in complex develop- strate pathways. On the other hand, recent developmental studies mental sequences. These constraints often allow one to infer suggest that a few entirely new substrate pathways have arisen evolutionary history from a comparison of extant chains of de- during evolution; these apparently provided opportunities for the velopmental events in various organisms (29-32). Such formation of completely new axon tracts. The corpus callosum, em- which is found only in placental mammals, may be such a truly bryological analyses of evolution-"ontophyletic analyses"-fo- new axon tract. We propose that the evolution of the corpus cal- cus on the ways that extant developmental sequences limit and losum is founded on the emergence of a new preaxonal substrate channel evolution (32). Here, we present an ontophyletic anal- pathway, the "glial sling," which bridges the two halves of the em- ysis of the evolution of the corpus callosum. bryonic forebrain only in placental mammals. Clearly, the creation of the corpus callosum must have orig- inated in mutations of the genome. However, production of the Increases in the number of central nervous system (CNS) neu- mature corpus callosum involves the cooperation of the prod- rons and in the complexity of the synaptic neuropil characterize ucts of many genes (33), and some of the necessary develop- the vertebrate phylogeny (1, 2). These increases are usually mental interactions appear to be quite distant from the genome manifest as enlargements of specific CNS areas such as the cer- (34-37). Thus, those mutations that originally brought about ebellum, the tectum, and the cerebrum. Local enlargements the evolution of the corpus callosum undoubtedly modified can be attributed to focal increases in the dominant class of ver- certain complex developmental sequences, sequences played tebrate neurons-local circuit neurons-neurons with axons that out some "distance" from the transcription and translation of extend only short distances in the CNS before synapsing (1). individual proteins. Local areas of the CNS are connected by another important Which critical developmental events may have been modi- class of neurons-projection neurons-which send their axons fied during the evolution of the corpus callosum? The corpus along a few long stereotyped routes to target areas far from their callosum is an axon tract of projection neurons. Most projection cell bodies. The white matter of the vertebrate CNS is com- tracts appear to be organized along preexisting substrate path- posed largely of axon tracts of projection neurons, and many of ways-neural "highways" that guide growing axons during de- the same major axon tracts can be identified throughout the velopment. On the basis of recent embryological discoveries, vertebrates. Although the overall pattern of these major tracts we propose that the critical developmental changes underlying appears to have been conserved during evolution (2-8), there the evolution of the corpus callosum included the acquisition are some significant variations. Frequently, the compactness of of a new substrate pathway. To show that this was a likely course particular tracts varies, as in the spinal lemniscal tracts (2, 9- of events, we must first examine both the general role of sub- 11). In some cases, the particular stereotyped route taken by strate pathways in the development of CNS axon tracts and the homologous axons varies-e.g., the stereotyped routes of the specific constraints that substrate pathways impose on evolu- corticospinal tracts differ among most primates, ungulates, ro- tionary changes in nervous systems. dents, and marsupials (12-14). Moreover, a few major verte- brate axon tracts have appeared with no apparent precursors. Substrate pathways The most dramatic example is the (dorsal) corpus callosum, which is found only in placental mammals (15, 16). Axon guidance pathways appear to be important factors in or- The corpus callosum is a large interhemispheric commissure, ganizing the overall layout of axon tracts of projection neurons, and most axons of the corpus callosum interconnect homotopic such as the neurons of the two major cortical commissures-the neocortical areas (17-22). (See refs. 23-25 for exceptions to this corpus callosum and the anterior commissure (38-54). We have general rule.) Monotremes and marsupials have no dorsal cor- called these stereotyped axon pathways "substrate pathways." Descriptions of the normal development of the CNS have shown The publication costs of this article were defrayed in part by page charge that most vertebrate axon tracts are normally organized along payment. This article must therefore be hereby marked "advertise- ment" in accordance with 18 U.S.C. §1734 solely to indicate this fact. Abbreviation: CNS, central nervous system. 5936 Downloaded by guest on September 26, 2021 Evolution: Katz et al. Proc. Natl. Acad. Sci. USA 80 (1983) 5937 the processes of nonneuronal substrate cells: the primitive glia, continue growing along the external capsules and thence to their the radial glia, and the developing ependyma of the neural tube terminations in the contralateral cortex. (43-54). (For a similar observation in amphioxus, see ref. 55.) The substrate pathway underlying the anterior commissure These descriptions suggest that the earliest substrate pathways is probably a common feature of the vertebrate ontogeny, be- followed by CNS axon tracts may be formed, at least in part, cause the anterior commissure is a constant feature of the ver- by ordered sets of nonneuronal cell processes. tebrate forebrain (2, 3, 15, 26, 66-75). In mammals lacking a The substrate pathways of the CNS seem to act as common corpus callosum (nonplacental mammals), the anterior com- highways between the cell bodies (NUC in Fig. 1) of projection missure increases in size as the neocortex increases (15, 28). neurons and the axon target areas (TA in Fig. 1) (42). During This suggests that during evolution an increasing number of development, those axons that will form the axon tracts usually axons have used the same underlying anterior commissure sub- grow from groups of immature neurons clustered in repro- strate pathway. We propose that the comparative ontogeny of ducible locations (NUC in Fig. 1) along the intermediate zone the anterior commissure reveals one of the major mechanisms of the developing neural tube (56-59). The first pioneer axons of axon tract evolution. An increased (or a decreased) use of a grow out singly or in small bundles along the early substrate constant preexisting substrate pathway appears to be a common pathways formed by the peripheral processes of particular non- mode of axon tract evolution, as can also be seen in the phy- neuronal substrate cells (47-54, 60), and the early substrate logenies of the corticospinal tracts (76) and the dorsal columns pathways are probably equivalent to the first marginal zones of (10). On the other hand, this mechanism cannot account for the the CNS (54). Subsequent axons appear to fasciculate along evolution of completely new axon tracts. What mechanisms may preexisting axons, and in the developing tracts new axons con- have been responsible for the evolution of those axon tracts, tinue to be added in successive layers to the preexisting bundles such as the corpus callosum, that have emerged without ob- (46-51, 60-63). In this way, the longitudinal pattern of the CNS vious antecedents? axon tracts is largely determined by the pattern of the early substrate pathways, while the radial pattern within an axon tract The corpus callosum develops along a new interhemispheric is largely determined by the sequence of addition of axons. Fi- substrate pathway nally, when reaching an appropriate target area (TA in Fig. 1), an axon probably follows local chemical cues and turns from the Recent embryological studies have shown that the first step in substrate pathway that it has been following (64, 65). the formation of the corpus callosum is a fusion of the two cere- bral hemispheres along the midline
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