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Neocortex: Origins 43 Neocortex: Origins 43 Neocortex: Origins F Aboitiz, Pontificia Universidad Cato´lica de Chile, structure, consisting of six laminae that remain some- Santiago, Chile what conserved across species and cortical regions. ã 2009 Elsevier Ltd. All rights reserved. Furthermore, it is subdivided into several distinct areas in the tangential domain, some of them being sensory, others motor, and still others receiving multi- modal input. In several mammalian groups there is a Introduction clear trend of tangential neocortical expansion that The origin of the mammalian neocortex is probably results in the increase of both surface area (leading to one of the most controversial themes in modern the formation of fissures and convolutions) and the comparative neurobiology. There have been long- number of cortical areas. The neocortex receives most standing arguments on this issue (dating from early of its extrinsic input from dorsal thalamic nuclei, last century), and still there is no general consensus many of them conveying sensory information from about it. This is partly due to the enormous anatomi- somatosensory, auditory, or visual modalities, and cal diversification that is observed in the cerebral projects back to the thalamus, to the amygdala, to hemispheres of distinct vertebrate groups. Starting the entorhinal cortex (which in turn projects to the from a relatively conserved embryonic plan that hippocampus), and to several subcortical structures, divides the hemispheres into a dorsal pallium and a including the spinal cord. ventral subpallium, different brain components have expanded in each vertebrate class, producing pro- Historical Background found distortions of the ancestral adult condition. For example, cartilaginous fishes are characterized Early in the last century, concepts on the evolution of by the development of a central pallial nucleus located the amniote brain (i.e., reptiles, birds, and mammals) at the dorsal midline, while bony fish develop a were dominated by Elliot Smith’s interpretation that brain in which the ventricular region everts to the sauropsids were characterized by the expansion of outside, separating the medial hemispheres in subpallial structures like the basal ganglia, leading the dorsal aspect. Amphibians possess quite a simple to the development of the DVR. On the other brain with little neuronal migration outside the in- hand, mammals would have expanded the pallial re- ternal ventricular zone, and almost no expansion of gion, producing the neocortex. Interestingly, other cell masses. Their pallium has been subdivided into authors, such as Nils Holmgren and Bengt Ka¨lle´n, medial, dorsal, and lateral components. On the proposed a pallial origin for the reptilian DVR, other hand, the pallium of reptiles and birds (saur- which they described as arising from a deep prolifera- opsida) displays a cortical, laminated architecture tive region that overlaps with the lateral cortex. containing a medial/dorsomedial (hippocampal) cor- Holmgren termed this region as the hypopallium, tex, a lateral (olfactory) cortex, and a small dorsal and considered it to be related to deep-brain mamma- cortex interposed between these two (in birds, the lian structures like the claustrum or parts of the amyg- region corresponding to the dorsal cortex has been dalar complex. However, these views were eclipsed by termed the Wulst, or more recently, the hyperpallium). Elliot Smith’s claim for a subpallial origin of the DVR. These components correspond to the different pallial Subsequent analyses performed in the 1970s, taking subdivisions in amphibians. In addition, the brains of advantage of newly developed histochemical proce- sauropsids display a conspicuous nuclear structure that dures, revealed that the reptilian DVR does not con- bulges into the ventricle, the dorsal ventricular ridge tain acetylcholinesterase activity as the basal ganglia (DVR), which receives many thalamic sensory projec- do, and is therefore a pallial structure. Furthermore, tions (Figure 1). tract-tracing experiments performed by Harvey Karten Mammals are characterized by the presence of a and collaborators, showed that the avian DVR (more neocortex (Figure 1). This structure is bound medially specifically, its anterior part, ADVR, or nidopallium) by the medial cortex or hippocampus, and laterally by received thalamic sensory projections similar to those the lateral or olfactory cortex. Deep to some cortical reaching some parts of the mammalian neocortex. areas like the insular region there are structures More precisely, collothalamic nuclei (i.e., thalamic such as the claustral complex. These and other dorsal nuclei receiving input from mesencephalic sensory structures make up the pallium, while the ventral centers, conveying visual and auditory information) subpallium includes the basal ganglia and related project to the ADVR/nidopallium of birds, and to the nuclei. The neocortex of mammals is indeed a unique lateral neocortex of mammals (visual extrastriate and 44 Neocortex: Origins Reptiles Mammals Neocortex Avian DVR DC NCd H NC M I DVR II–III HIP NCI IV MC CL N En LC CS V–VI CS OC White matter AM Arc P R Figure 1 The cerebral hemispheres of reptiles and mammals. In Figure 2 Harvey Karten’s original cell-equivalent hypothesis, the dorsal aspect of the hemisphere, reptiles display a cortex, with in which visual processing circuits of the avian nidopallium (N) medial/dorsomedial (MC), dorsal (DC), and lateral (LC) compo- and arcopallium (Arc) are homologous to those of the different nents, and a dorsal ventricular ridge (DVR) consisting of an ante- layers in the mammalian extrastriate visual cortex. En, entopal- rior part and a posterior part (not shown). The anterior DVR lium (a component of the nidopallium); H, hyperpallium; M, meso- receives most sensory projections from mesencephalic-receiving pallium; P, pulvinar nucleus; R, rotundus nucleus. thalamic nuclei. The medial and dorsomedial cortices of reptiles (MC) have been compared to the hippocampal formation (HIP) of mammals, and the lateral cortex (LC) is considered homologous dorsal cortex, which is located in a similar relative to the mammalian olfactory cortex (OC). The dorsal cortex (DC) of position as the neocortex: interposed between the reptiles has characteristics of both the entorhinal cortex (adjacent lateral (olfactory) and the medial (hippocampal) cor- to the hippocampal formation; not shown) and the neocortex (NC) of mammals. The latter appears subdivided into a dorsal aspect, tices. Thus, in the origin of mammals, collothalamic NCd, and a lateral aspect, NCl. There is no consensus regarding projections originally destined to the ADVR or its the homology of the anterior DVR. According to some authors, this equivalent region might have deviated or sent collat- structure corresponds to the mammalian lateral neocortex (NCl), erals toward an expanding dorsal pallium or dorsal while others consider that it relates to the claustroamygdaloid cortex. This change was considered to be more likely complex (AM, CL). Reproduced from Northcutt RG and Kaas JH (1995) The emergence and evolution of mammalian neocortex. to occur than a transformation of the topographic Trends in Neuroscience 18: 373–379, with permission from positions of the embryonic proliferative zones and Elsevier. the adult structures. Supporting this view, the mam- malian neocortex bears other patterns of connectivity auditory cortices). On the other hand, lemnothalamic that are not found in sauropsids, like the interhemi- nuclei (receiving direct sensory input from ascending spheric connections and the corticospinal tract. This lemniscal systems, carrying visual or somatosensory is to be expected from a structure that increases in size input) project to the avian hyperpallium, and to the and consequently increases its connectivity domains. dorsal neocortex of mammals (primary visual and Additional considerations on the topography, devel- somatosensory cortices). Thus, Karten proposed that opment, and connectivity of the sauropsidian ADVR the avian hyperpallium (dorsal cortex of reptiles) led to the revival of Holmgren’s hypothesis of was homologous to the dorsal neocortex of mam- homology between this structure and either the dorsal mals (both receiving lemnothalamic input), while the claustral complex or the basolateral amygdala of ADVR/nidopallium of birds and reptiles was homolo- mammals. gous to the mammalian lateral neocortex (both receiv- ing collothalamic input). Furthermore, relying on Developmental and Genetic Evidence similarities in intrinsic connectivity, it was proposed that different components of the avian ADVR corre- An important breakthrough in this controversy was sponded to specific neocortical layers in mammals provided by the analysis of regulatory gene expres- (Figure 2). sion patterns in the developing telencephalon, which This hypothesis dominated the views of early mam- identified three main compartments during the speci- malian brain evolution and neocortical origins for fication of the cerebral vesicles: the subpallium, being several years. Nevertheless, there were always some positive for regulatory genes such as Dlx1 and Dlx2; dissenters, backed by the early embryological studies the medial, dorsal, and lateral pallia (or medial, and by the different topographical position of the dorsal, and lateral cortices), expressing genes such mammalian neocortex and the reptilian DVR. In as Emx1, Tbr1, and Pax6; and the intermediate terri- these alternative views, the most likely homolog of tory
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