5384204 Brain Segmentation and Forebrain Development in Amniotes

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Brain Research Bulletin, Vol. 55, No. 6, pp. 695710, 2001 Copyright 2001 Elsevier Science Inc. Printed in the USA. All rights reserved 0361-9230/01/$see front matter

PII S0361-9230(01)00588-3

Evolution of the Nervous System

Brain segmentation and forebrain development in amniotesLuis Puelles* Department of Morphological Sciences, University of Murcia, Murcia, SpainABSTRACT: This essay contains a general introduction to the segmental paradigm postulated for interpreting morphologically cellular and molecular data on the developing forebrain of vertebrates. The introduction examines the nature of the problem, indicating the role of topological analysis in conjunction with analysis of various developmental cell processes in the developing brain. Another section explains how morphological analysis in essence depends on assumptions (paradigms), which should be reasonable and well founded in other research, but must remain tentative until time reveals their necessary status as facts for evolving theories (or leads to their substitution by alternative assumptions). The chosen paradigm affects many aspects of the analysis, including the sectioning planes one wants to use and the meaning of what one sees in brain sections. Dorsoventral patterning is presented as the fundament for dening what is longitudinal, whereas less well-understood anteroposterior patterning results from transversal regionalization. The concept of neural segmentation is covered, rst historically, and then step by step, explaining the prosomeric model in basic detail, stopping at the diencephalon, the extratelencephalic secondary prosencephalon, and the telencephalon. A new pallial model for telencephalic development and evolution is presented as well, updating the proposed homologies between the sauropsidian and mammalian telencephalon. 2001 Elsevier Science Inc. KEY WORDS: Prosomeric model, Forebrain, Patterning, Segmentation, Neuromeres, Longitudinal zones, Histogenesis, Migration, Diencephalon, Telencephalon, Pallium, Subpallium.

INTRODUCTION Amniote vertebrates include reptiles, birds, and mammals. Stem reptiles clearly were ancestral to all present amniote forms, and derived from anamniote amphibian stock. It is still being discussed which is the correct evolutionary branching schema among amniotes. Turtles are thought to be closest to both stem reptiles and stem mammals, and crocodiles, jointly with extinct dinosaurs, closest to birds, which agrees with data on brain morphology (see [87] for a modern molecular viewpoint). The amniote forebrain is notoriously complex and therefore there is no easy way to approach its development. I will not deal here with neural induction, early regional patterning, and clonal

growth previous to neurulation. These fundamental processes show substantial topological, cellular, and molecular similarities when studied across vertebrates (for review see [73]). In trying to understand forebrain development and evolution, I have come to favor a threefold approach, which involves topological analysis of form and structure, causal cellular mechanisms, and molecular fundaments. The last two lines of research are pursued abundantly in current developmental literature, but topological analysis remains largely a solitary endeavor, owering exceptionally here and there. Still, I believe it is an all important line because topology of form and structure gives critical contextual (positional) meaning to cellular interactions and molecular function. It is of no use to simplify excessively or forget this aspect. Of course, in the brain, form and structure means the shape and building blocks of the walls of the neural tube, and these evolve variously in three dimensions during both ontogenesis and phylogenesis. The hollow shape of the neural tube is a topological onemany transform of the neural plate shape (Figs. 1A,B) as indicated by fate-mapping studies [16,34,56,73]. A one-many transform means that, growth being implied, each small primordium (cell group or individual cell) gives rise to a larger derivative (or clone), but the overall topology of parts does not change. Later, differential growth and differentiation processes introduce other site-specic topological transformations (i.e., evagination of the telencephalic hemispheres; Fig. 1D). In essence, regionalized distinct elds of the primitive neural tube wall each give rise to a tridimensional radial complex of neural structures in the mature brain, stretching from the ventricular surface to the pial surface (Figs. 1C,D). Eventually, some of the cell populations originated within one radial histogenetic complex migrate tangentially, colonizing other radial complexes (arrow T in Fig. 1D; [1,2,49]). This usually affects the grain or structure of the brain wall, but not so much its form, at least in the forebrain. Some tangential migrations in the hindbrain do affect its form (i.e., the rhombic lip migrations). Cell groups found at each site of the neural tube wall thus in principle have formal relationships along three dimensions: DV, anteroposterior, and radial (ventriculo-pial, or inside-out) (Fig. 1). Understanding of local brain morphogenesis therefore involves

* Address for correspondence: Luis Puelles, Department of Morphological Sciences, Faculty of Medicine, University of Murcia, 30100 Murcia, Spain. Fax: 34-968-363955; E-mail: puelles@um.es

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FIG. 1. Schemata illustrating the topological radial structure and relative dorsoventral (DV) dimensions of the neural plate and tube. (A) Neural plate cross-section and direction of neurulation deformation. (B) Neural tube, overlying neural crest and skin. (C) Neural tube cross-section at a more advanced stage of development, showing differential mass of ventricular zone neuroepithelium (inverse to differentiated state) and radial migration routes of alar and basal neuroblasts into the forming mantle layer. Arrows D/V indicate dorsal and ventral directions. (D) Schema of more complex forebrain area, including the evaginating telencephalon (section plane indicated in Fig. 6). Note advanced regionalization, particularly of the alar plate, and the diverse topography in each part of the topologically invariant radial dimension (unlabeled arrows). For comparison, arrows labeled D or V indicate the deformed dorsoventral dimension and arrow T symbolizes what would represent a supercial tangential migration. Abbreviations used in gures: A, anterior; Aa, anterior archistriatum (part of avian amygdala); ac, anterior commissure; ACC, nucleus accumbens (striatal); AEP, anterior entopeduncular area; AH, anterior hypothalamus; Aid, intermedio dorsal archistriatum (part of avian amygdala); Aiv, intermedio ventral archistriatum (part of avian amygdala); AMYGD amygdala; AON, anterior olfactory nucleus; AP, alar plate; Ap posterior archistriatum (part of avian amygdala); BL, basolateral amygdaloid nucleus; BM, basomedial amygdaloid nucleus; BP, basal plate; BST, bed nucleus stria terminalis; BSTA, anterior bed nucleus stria terminalis; BSTP, posterior bed nucleus stria terminalis; C, central amygdaloid nucleus; ca, anterior commissure; Cb, cerebellum; CENT, central; cf, cephalic exure; ch, choroidal roof tissue; CLdl, dorsolateral claustrum; CLvm, ventromedial claustrum; cp, pallial/hippocampal commissure; CX, cortex; D, dorsal; DBH, diagonal band, horizontal part; DBV, diagonal band, vertical part; DH, dorsal hypothalamus; Di, diencephalon; DP, dorsal pallium; DT, dorsal thalamus; DVR, dorsal ventricular ridge; EMT, eminentia thalami; Ep, endopiriform nucleus; EP, epiphysis; m, mbria hippocampi; FP, oor plate; Hab, habenula; hc, hippocampal commissure; HP, neurohypophysis; HV, hyperstriatum ventrale (dorsal part of avian DVR LP); IC, internal capsule; IH, infundibular hypothalamus; IIIv, third ventricle; Is, isthmus; ivf, interventricular foramen; L, lateral amygdaloid nucleus; LGE/ST, lateral ganglionic eminence (striatum); lot, lateral olfactory tract; LP, lateral pallium; M, midbrain; Mam, mammillary region; Me, medial amygdaloid nucleus; MES, mesencephalon; MGE/BST, medial ganglionic eminence (supracapsular bed nucleus of stria terminalis); MGE/PAL, medial ganglionic eminence (pallidum); MP, medial pallium; mz, mantle zone; N, neostriatum (ventral part of avian DVR VP); NC, notochord; NCL, neostriatum caudolaterale (part of neostriatum); OB, olfactory bulb; och, optic chiasm; os, optic stalk; P, posterior; p1p6, prosomeres 1 6; PAL, pallidum; Palio, pallium; PAL-S, pallidal septum; PO, preoptic region; POA, anterior preoptic area; PP,

AMNIOTE FOREBRAIN DEVELOPMENT visualizing six neighborhood relationships (rostral, caudal, dorsal, ventral, inner, and outer) in causal morphospace. To this must be added known instances of tangential migration, which relocate cells from one topological locus into another (and other invasive phenomena, like vascularization and colonization by blood-borne microglia cells). Fortunately, at the beginning, important changes may affect preferentially one structural dimension, allowing us to momentarily consider the other dimensions as relatively unchanged. Dorsoventral (DV) patterning causes longitudinal zonation in the forebrain and elsewhere in the brain, which is topologically similar to a closed cylinder. This I regard as one of the earliest regionalization effects, immediately consequent to planar induction effects before and during gastrulation (Fig. 2; see [13,19,75]). Classically, planar induction has been described to affect only the anteroposterior (AP) pattern [15]. AP patterning leads to major brain parts (tagma), secondary organizers (like the isthmic organizer, or the thalamic zona limitans), segmentation inside tagma (metamera or neuromeres), and transverse regionalization in general. Note that mixed DV/AP effects may generate later some oblique patterns (see, e.g., [68]). Finally, later radi