Cholinergic innervation of the frontal cortex: differences among humans, chimpanzees, and macaque monkeys.

Cholinergic innervation of the frontal cortex is important in higher cognitive functions and may have been altered in humans relative to other species to support human-specific intellectual capacities. To evaluate this hypothesis we conducted quantitative comparative analyses of choline acetyltransferase-immunoreactive axons in cortical areas 9, 32, and 4 among humans, chimpanzees, and macaque monkeys. Area 9 of the dorsolateral prefrontal cortex is involved in inductive reasoning and specific components of working memory processes, while area 32 of the medial prefrontal cortex has been implicated in theory of mind. Area 4 (primary motor cortex) was also evaluated because it is not directly associated with higher cognitive functions. The findings revealed no quantitative species differences in the three cortical areas examined, indicating that human cognitive specializations are not related to a quantitative increase in cortical cholinergic input. However, species-specific morphological specializations were observed. Clusters of cholinergic fibers that may be indicative of cortical plasticity events were present in chimpanzees and humans, but not in macaques. The other significant morphology noted was the common and distinctive oval or ovoid perisomatic staining in macaque cortices. This feature was also sporadically observed in chimpanzee cortex. Our findings suggest a potential alteration of cortical cholinergic afferents within the prefrontal cortex of humans and chimpanzees, to the exclusion of macaque monkeys.

Cortical orofacial motor representation in Old World monkeys, great apes, and humans. II. Stereologic analysis of chemoarchitecture.

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.