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3.08 the Evolution of Neuron Classes in the Neocortex of Mammals 3.08 The Evolution of Neuron Classes in the Neocortex of Mammals P R Hof, Mount Sinai School of Medicine, New York, NY, USA C C Sherwood, The George Washington University, Washington, DC, USA ª 2007 Elsevier Inc. All rights reserved. 3.08.1 Introduction 114 3.08.2 Neuronal Typology and Chemical Specialization 114 3.08.2.1 Pyramidal Neurons 114 3.08.2.2 Spiny Stellate Cells 116 3.08.2.3 Inhibitory Interneurons: Basket, Chandelier, and Double Bouquet Cells 116 3.08.3 Relationships of Neurochemical Phenotype and Phylogenetic Affinities 117 3.08.3.1 General Phylogenetic Patterns 117 3.08.3.2 The Distribution of Some Neuron Classes Closely Matches Phylogenetic Affinities 118 3.08.3.3 Other Phylogenetic Distributions of Cortical Neuron Classes Indicate Convergent Evolution 120 3.08.4 Functional Considerations 121 Glossary Hominidae A primate clade that includes great apes (orangutans, gorillas, chimpan- Afrotheria A clade of placental mammals that is zees, and bonobos) and humans. The thought to have originated in Africa at hylobatids (gibbons and siamangs) a time when it was isolated from other are the sister taxon to the Hominidae. continents. This clade contains homoplasy A structure that is the result of con- Paenungulata (elephants, hyraxes, and vergent evolution, where organisms sirenians), Afrosoricida (tenrecs and that are not closely related indepen- golden moles), Tubulidentata (aard- dently acquire similar characteristics. varks), and Macroscelidea (elephant Homoplasy is contrasted with shrews). Molecular data indicate that homology, which means that struc- the Afrotheria diverged from other pla- tures have a common origin derived cental mammals 110–100 Mya. from a shared ancestor. Anthropoidea A primate clade that includes New Laurasiatheria A supraordinal clade of boreo- World monkeys, Old World mon- eutherian placental mammals that keys, apes, and humans. Tarsiers are includes Cetartiodactyla, Perisso- the sister group to the Anthropoidea. dactyla, Carnivora, Pholidota, and Boreoeutheria A clade of placental mammals that Eulipotyphla. encompasses Euarchontoglires and marsupials A clade of mammals in which the Laurasiatheria. This taxonomic divi- female has a pouch where the young is sion within the Boreoeutheria nurtured through early infancy. There occurred 95–85 Mya in the Cretaceous. are approximately 280 species of living Cetartiodactyla A clade of placental mammals that marsupials, with the majority being includes cetaceans (whales, dolphins, native to Australia and the remainder and porpoises) and artiodactyls living in South America (however, there (even-toed ungulates). This phyloge- is a single North American native mar- netic grouping is based on molecular supial species, the Virginia opossum). evidence indicating that cetaceans monotremes A clade of mammals that lay eggs, evolved from within the artiodactyls rather than giving birth to live young and have their closest relationship like marsupials and placental mam- with the hippopotamus and then mals. The extant representatives of ruminants (cattle and deer). this group, the platypus and the echid- Euarchontoglires A supraordinal clade of boreoeuther- nas, are indigenous to Australia, New ian placental mammals that includes Guinea, and Tasmania. Fossil evidence, Rodentia, Lagomorpha, Dermoptera, however, suggests that monotremes Scandentia, and Primates. were once more widespread. 114 The Evolution of Neuron Classes in the Neocortex of Mammals placental A clade of mammals in which the these cellular phenotypes could be used to assess mammals fetus is nourished during gestation taxonomic affinities and functional differences by a placenta. This group encom- among species. passes the majority of living mammals. Xenarthra A clade of placental mammals pre- 3.08.2 Neuronal Typology and Chemical sent today only in the Americas. This group includes sloths, anteaters, Specialization and armadillos. Molecular data indi- 3.08.2.1 Pyramidal Neurons cate that the Xenarthra diverged from boreoeutherian mammals Pyramidal neurons are the principal excitatory 100–95 Mya. neuronal class in the cerebral cortex. They are highly polarized neurons, with a major orientation axis orthogonal to the pial surface of the cerebral 3.08.1 Introduction cortex. Their cell body is roughly triangular on cross section, although a large variety of morpho- A diverse array of neuron types populates the logic types exist with elongate, horizontal or mammalian neocortex. Physiological activity vertical fusiform, or inverted perikaryal shapes. within a cortical area, in turn, is largely deter- They typically have a large number of dendrites mined by interactions among these different cell that emanate from the apex and from the base of types and incoming afferents. Neurons in the cer- the cell body. The span of their dendrites may ebral cortex of mammals can be divided into two cover several millimeters and their somata are major classes on the basis of morphology and found in all cortical layers except layer I, with function, pyramidal excitatory cells, and inhibi- predominance in layers II, III, and V. Small pyr- tory interneurons. Each class includes many amidal neurons in layers II and III of the subtypes that can be identified by their size, neocortex have a restricted dendritic tree and shape, dendritic and axonal morphology, and con- form vast arrays of axonal collaterals with neigh- nectivity. These neuronal subtypes exhibit a boring cortical domains, whereas medium to large variable distribution among cortical layers and pyramidal cells in deep layer III and layer V have regions, and some are differentially represented a much more extensive dendritic tree and furnish among species (see Hof et al., 1999, 2000; Hof long corticocortical connections. Layer V also and Sherwood, 2005). Neurons can be further contains very large pyramidal neurons disposed classified based on their expression of various in clusters or as isolated, somewhat regularly proteins, such as neurofilament proteins (NFPs), spaced elements. These neurons are known to calcium-binding proteins, and neuropeptides. project to subcortical centers such as the basal The morphology of a given neuron, particularly ganglia, brainstem, and spinal cord. Finally, layer of its dendritic arborizations, reflects the size of its VI pyramidal cells exhibit a greater morphologic receptive field and the specificity of its synaptic variability than those in other layers, and are contacts. Thus, the structure of the dendritic involved in certain corticocortical as well as corti- arbor as well as the distribution of axonal terminal cothalamic projections. The dendrites of ramifications confer a high level of subcellular spe- pyramidal cells show large numbers of dendritic cificity in the localization of particular synaptic spines that receive most of the excitatory synaptic contacts on a given neuron. The three-dimensional inputs. As many as 40 000 spines can be encoun- distribution of the dendritic tree is also a key factor tered on a large pyramidal neuron. with respect to the type of information transferred The major excitatory output of the neocortex is to the neuron. A neuron with a dendritic tree furnished by pyramidal cells. Their axon extends in restricted to a particular cortical layer may be most cases from the base of the perikaryon and receptive to a very limited pool of afferents, courses toward the subcortical white matter and whereas widely expanding dendritic branches typi- gives off several collateral branches that are direc- cal of large pyramidal neurons will receive highly ted to cortical domains generally located within the diversified inputs in the cortical layers through vicinity of the cell of origin. While many of these which the dendrites course. Considering the varia- branches ascend in a radial, vertical pattern of bility in cortical morphology, size, and cellular arborization, a separate set of projections also tra- organization in mammals, it is important to inves- vels horizontally over long distances. One function tigate how specific characteristics of cortical of the vertically oriented component of the recur- microcircuitry differ among species, and how rent collaterals may be to interconnect layers III The Evolution of Neuron Classes in the Neocortex of Mammals 115 and V, the two major output layers of the neocor- highly specific long corticocortical projections, and tex. Horizontal intrinsic connections are positioned show regional specificity in their distribution pat- to recruit and coordinate the activity of modules of terns (Campbell and Morrison, 1989; Campbell similar functional properties while inhibiting other et al., 1991; Hof and Nimchinsky, 1992; domains. Together these recurrent projections Carmichael and Price, 1994; Hof and Morrison, function to set up local excitatory patterns and 1995; Hof et al., 1995b; Nimchinsky et al., 1995, coordinate the output of neuronal ensembles. 1996, 1997; Preuss et al., 1997, 1999; Sherwood NFP immunoreactivity, chiefly recognized by the et al., 2003a; Vogt et al., 2001, 2005). Although expression of dephosphorylated epitopes of NFP the precise function of NFP is not completely medium and heavy molecular weight subunits, understood, its restricted distribution among cer- characterizes a subpopulation of pyramidal neu- tain subsets of corticocortical circuits in primates rons in the neocortex of mammals that exhibits suggests that it confers unique neurochemical and clear regional and species differences in their dis- morphologic properties subserving a range
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