Cortical Orofacial Motor Representation in Old World Monkeys, Great Apes, and Humans

Abstract

This study presents a comparative stereologic investigation of neurofilament protein- and calcium-binding protein-immunoreactive neurons within the region of orofacial representation of primary motor cortex (Brodmann’s area 4) in several catarrhine primate species (Macaca fascicularis, Papio anubis, Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, and Homo sapiens). Results showed that the density of interneurons involved in vertical interlaminar processing (i.e., calbindin- and calretinin-immunoreactive neurons) as well pyramidal neurons that supply heavily-myelinated projections (i.e., neurofilament protein-immunoreactive neurons) are correlated with overall neuronal density, whereas interneurons making transcolumnar connections (i.e., parvalbumin-immunoreactive neurons) do not exhibit such a relationship. These results suggest that differential scaling rules apply to different neuronal subtypes depending on their functional role in cortical circuitry. For example, cortical columns across catarrhine species appear to involve a similar conserved network of intracolumnar inhibitory interconnections, as represented by the distribution of calbindin- and calretinin-immunoreactive neurons. The subpopulation of horizontally-oriented wide-arbor interneurons, on the other hand, increases in density relative to other interneuron subpopulations in large brains. Due to these scaling trends, the region of orofacial representation of primary motor cortex in great apes and humans is characterized by a greater proportion of neurons enriched in neurofilament protein and parvalbumin compared to the Old World monkeys examined. These modifications might contribute to the voluntary dexterous control of orofacial muscles in great ape and human communication.

Neocortical neuron types in Xenarthra and Afrotheria: implications for brain evolution in mammals

“…These results challenge the proposition that there is a canonical inhibitory interneuron network that is relatively invariant across species and cortical areas, as has been previously suggested (Clemo et al 2003;Douglas and Martin 2004;Hendry et al 1987;Nelson et al 2006;Silberberg et al 2002). In fact, many authors have commented on phylogenetic diversity in the distribution of neocortical inhibitory interneurons among mammalian species (Ballesteros-Yañez et al 2005;DeFelipe et al 2002;Glezer et al 1993;Hendry and Carder 1993;Hof et al 1999;Hof and Sherwood 2005;Preuss and Coleman 2002;Sherwood et al 2004. Specifically, comparative quantitative studies indicate that the overall percentage of GABAergic interneurons within the neocortex is greater in cetaceans than in rodents and primates (Glezer et al 1993;Hof et al 2000), and even greater still in primates compared to rodents (DeFelipe et al 2002;del Rio and DeFelipe 1996;Gabbott and Bacon 1996;Gabbott et al 1997;Gonchar and Burkhalter 1997).…”

“…There was considerable regional variation in the density of these CBir presumptive projection neurons in layers II-III, with the highest frequencies found in frontal cortex, insular cortex, primary somatosensory cortex, primary motor cortex, and visual cortex. CB-ir pyramidal neurons have been similarly reported in layers II-III of rodents (Andressen et al 1993;Desgent et al 2005;Gonchar and Burkhalter 1997;Van Brederode et al 1991), primates (Hof and Morrison 1991; Kondo et al 1999;Sherwood et al 2004, megachiropterans, perissodactyls, and cetartiodactyls ). In addition, CB-ir atypical pyramidal neurons have been described in layer IIIc/V of the visual cortex of cetaceans, including inverted pyramidal neurons (Glezer et al 1993).…”

“…The laminar pattern of staining in atlantogenatans most closely resembles the monotreme echidna (Hassiotis et al 2005) and the marsupial tammar wallaby , but differs from the distribution pattern of NPNFP-ir neurons in layer III, V, and VI throughout the neocortex which characterizes most other eutherians (Baldauf 2005;Boire et al 2005;Bourne et al 2005Bourne et al , 2007Budinger et al 2000;Campbell and Morrison 1989;Chaudhuri et al 1996;Hof et al 1996a;Hof and Sherwood 2005;Nimchinsky et al 1997;Preuss et al 1997;Sherwood et al 2004;Tsang et al 2000;Van der Gucht et al 2007.…”

“…These cells had round or ovoid somata with proximal dendrites oriented in an axis parallel to the pia. Cajal-Retzius cells that express CR are known from many other mammals (Cruikshank et al 2001;Glezer et al 1998;Gonchar and Burkhalter 1999;Hassiotis et al 2005;Hof et al 1999;Schwark and Li 2000;Sherwood et al 2004). Although there was generally not very intense CR staining of the neuropil, the detectable immunoreactive fibers were beaded and usually had a vertical orientation (Fig.…”

Face to face with the social brain

“…This is due in part to the overall similarity of the muscles of facial expression across primates [16 -21]. In contrast to the apparent conservatism of facial display types in anthropoids, the degree of neural control over the muscles of facial expression appears to be much more variable between species [22][23][24][25][26], and is therefore amenable to comparative analysis.…”