Evolution of the amniote pallium and the origins of mammalian neocortex

Abstract

Karten's neocortex hypothesis holds that many component cell populations of the sauropsid dorsal ventricular ridge (DVR) are homologous to particular cell populations in layers of auditory and visual tectofugal-recipient neocortex of mammals (i.e., temporal neocortex), as well as to some amygdaloid populations. The claustroamygdalar hypothesis, based on gene expression domains, proposes that mammalian homologues of DVR are found in the claustrum, endopiriform nuclei, and/or pallial amygdala. Because hypotheses of homology need to account for the totality of the evidence, the available data on multiple forebrain features of sauropsids and mammals are reviewed here. While some genetic data are compatible with the claustroamygdalar hypothesis, and developmental (epigenetic) data are indecisive, hodological, morphological, and topographical data favor the neocortex hypothesis and are inconsistent with the claustroamygdalar hypothesis. Detailed studies of gene signaling cascades that establish neuronal cell-type identity in DVR, tectofugal-recipient neocortex, and claustroamygdala will be needed to resolve this debate about the evolution of neocortex.

Figure 1

Photomicrographs of Nissl-stained hemisections through the telencephalon, rostral to caudal as A–C, with mirror-image line drawings. The visual thalamofugal projection from the dorsal lateral geniculate nucleus to the Wulst (hyperpallium) is shown in A (the comparable somatosensory pathway to the Wulst is rostral to the level shown here). The visual tectofugal pathway via nucleus rotundus to the entopallium is shown in A and B, and the auditory tectofugal pathway via nucleus ovoidalis to field L is shown in C. Abbreviations: CM, caudal mesopallium; E, entopallium; Ep, perientopallium; H, hippocampal formation; L1, field L1 pallii; L2, field L2 pallii; L3, field L3 pallii; M, mesopallium; N, nidopallium; Nc, nidopallium caudale; W, Wulst (hyperpallium). The subpallium is indicated by shading.

Figure 2

Summary diagram of the type I bottlebrush tectothalamic neuron pathway in mammals (A, based on work in ground squirrels) and birds (B, based on work in pigeons and chickens) from Major et al. The schematic shows the high similarity in neuronal morphology of these neuron types in mammals and birds. Additionally, the circuitry of this neuron type shows many similarities between birds and mammals, including (1) the inputs from W-type retinal ganglion cells (RGCs) and from cholinergic neurons of the parabigeminal nucleus in mammals and nucleus isthmi parvocellularis (Ipc) in birds; (2) an output to a thalamic cell group projecting to a visual processing region of the temporal telencephalic pallium (caudal/inferior pulvinar in mammals and nucleus rotundus in birds); and (3) an output to a GABAergic pretectal cell group(s) projecting to the thalamic target of the type bottlebrush neurons. Abbreviations: Ach, acetylcholine; GABA, gamma aminobutyric acid; Glut, glutamate; IPS, interstitio-pretecto-subpretectalis; NPA, anterior pretectal nucleus; NPP, posterior pretectal nucleus; NPT, nucleus pretectalis; PBG, parabigeminal nucleus; SP, nucleus subpretectalis; W RGCs, W-type retinal ganglion cells. Used with the kind permission of John Wiley and Sons.

Figure 3

Topological comparison of the pallial regions of a stem amniote, a generalized extant mammal, and a generalized extant sauropsid, as postulated by Butler. For this and subsequent figures, the medial pallium, i.e., hippocampal formation, is indicated by light shading, the lemnopallial regions in hatching from upper left to lower right, the collopallial regions in hatching from upper right to lower left, and the piriform cortex in darker shading. The same topological order holds across extant mammalian neocortex and the extant sauropsid dorsal cortex/Wulst and dorsal ventricular ridge sensory-recipient pallial regions. Abbreviations: A, auditory pallium; Ci, cingulate gyrus; Dl, dorsolateral pallium; Dml, lateral part of dorsomedial pallium; Dmm, medial part of dorsomedial pallium; F, frontal neocortex; I, insular cortex; P, piriform cortex; S, subiculum; SM, somatomotor cortex; V1, primary visual cortex; V2, secondary visual cortex. Where abbreviations for mammalian pallial terms, such as cingulate gyrus and insular cortex, are used in the sauropsid diagram, their respective homologues are indicated.

Figure 4

Comparison of Butler's, on the left, and Reiner's, on the right, postulated pallial components in the common stem amniote ancestor of the synapsid radiation leading to mammals and the diapsid radiation leading to sauropsids. Each figure illustrates a schematized transverse hemisection on the right side, with medial to the left. Reiner coined the term proto-DVR for the pallial region constituting V2 and A in sauropsids. As can be seen in comparing the two diagrams, Butler and Reiner agree that the initial pallial expansion of collothalamic-recipient regions was very small and constituted neither a full-blown DVR as seen in extant sauropsids nor a full-blown neocortex as seen in extant mammals. Abbreviations: A, primary auditory pallium; C, collopallium; H, hippocampal pallium; L, lemnopallium; P, piriform cortex; V1, primary visual pallium; V2, secondary visual pallium.