Comparative analysis of the nucleus basalis of Meynert among primates.

Long projection axons from the Ch4 cell group of the nucleus basalis of Meynert (nbM) provide cholinergic innervation to the neurons of the cerebral cortex. This cortical cholinergic innervation has been implicated in behavioral and cognitive functions, including learning and memory. Recent evidence revealed differences among primate species in the pattern of cholinergic innervation specific to the prefrontal cortex. While macaques displayed denser cholinergic innervation in layers I and II relative to layers V and VI, in chimpanzees and humans, layers V and VI were as heavily innervated as the supragranular layers. Furthermore, clusters of cholinergic axons were observed within the prefrontal cortex of both humans and chimpanzees to the exclusion of macaque monkeys, and were most commonly seen in humans. The aim of the present study was to determine whether the Ch4 cell group was modified during evolution of anthropoid primates as a possible correlate of these changes in cortical cholinergic innervation. We used stereologic methods to estimate the total number of choline acetyltransferase-immunoreactive magnocellular neurons within the nbM of New World monkeys, Old World monkeys, apes, and humans. Linear regression analyses were used to examine the relationship of the Ch4 cell group with neocortical volume and brain mass. Results showed that total nbM neuron numbers hyposcale relative to both neocortical volume and brain mass. Notably, the total number of nbM neurons in humans were included within the 95% confidence intervals for the prediction generated from nonhuman data. In conclusion, while differences in the cholinergic system exist among primate species, such changes appear to involve mostly axon collateral terminations within the neocortex and, with the exception of the relatively small group of cholinergic cells of the subputaminal subdivision of the nbM at the anterointermediate and rostrolateral levels, are not accompanied by a significant extra-allometric increase in the overall number of subcortical neurons that provide that innervation.

The influence of experimental manipulations on chewing speed during in vivo laboratory research in tufted capuchins (Cebus apella).

Even though in vivo studies of mastication in living primates are often used to test functional and adaptive hypotheses explaining primate masticatory behavior, we currently have little data addressing how experimental procedures performed in the laboratory influence mastication. The obvious logistical issue in assessing how animal manipulation impacts feeding physiology reflects the difficulty in quantifying mechanical parameters without handling the animal. In this study, we measured chewing cycle duration as a mechanical variable that can be collected remotely to: 1) assess how experimental manipulations affect chewing speed in Cebus apella, 2) compare captive chewing cycle durations to that of wild conspecifics, and 3) document sources of variation (beyond experimental manipulation) impacting captive chewing cycle durations. We find that experimental manipulations do increase chewing cycle durations in C. apella by as much as 152 milliseconds (ms) on average. These slower chewing speeds are mainly an effect of anesthesia (and/or restraint), rather than electrode implantation or more invasive surgical procedures. Comparison of captive and wild C. apella suggest there is no novel effect of captivity on chewing speed, although this cannot unequivocally demonstrate that masticatory mechanics are similar in captive and wild individuals. Furthermore, we document significant differences in cycle durations due to inter-individual variation and food type, although duration did not always significantly correlate with mechanical properties of foods. We advocate that the significant reduction in chewing speed be considered as an appropriate qualification when applying the results of laboratory-based feeding studies to adaptive explanations of primate feeding behaviors.

Species-specific distributions of tyrosine hydroxylase-immunoreactive neurons in the prefrontal cortex of anthropoid primates.

In this study, we assessed the distribution of cortical neurons immunoreactive for tyrosine hydroxylase (TH) in prefrontal cortical regions of humans and nonhuman primate species. Immunohistochemical methods were used to visualize TH-immunoreactive (TH-ir) neurons in areas 9 (dorsolateral prefrontal cortex) and 32 (anterior paracingulate cortex). The study sample included humans, great apes (chimpanzee, bonobo, gorilla, orangutan), one lesser ape (siamang), and Old World monkeys (golden guenon, patas monkey, olive baboon, moor macaque, black and white colobus, and François' langur). The percentage of neurons within the cortex expressing TH was quantified using computer-assisted stereology. TH-ir neurons were present in layers V and VI and the subjacent white matter in each of the Old World monkey species, the siamang, and in humans. TH-ir cells were also occasionally observed in layer III of human, siamang, baboon, colobus, and François' langur cortex. Cortical cells expressing TH were notably absent in each of the great ape species. Quantitative analyses did not reveal a phylogenetic trend for percentage of TH-ir neurons in these cortical areas among species. Interestingly, humans and monkey species exhibited a bilaminar pattern of TH-ir axon distributions within prefrontal regions, with layers I-II and layers V-VI having the densest contingent of axons. In contrast, the great apes had a different pattern of laminar innervation, with a remarkably denser distribution of TH-ir axons within layer III. It is possible that the catecholaminergic afferent input to layer III in chimpanzees and other great apes covaries with loss of TH-ir cells within the cortical mantle.

Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: a comparative study.

In this study, we assessed the possibility that humans differ from other primate species in the supply of dopamine to the frontal cortex. To this end, quantitative comparative analyses were performed among humans, chimpanzees, and macaques using immunohistochemical methods to visualize tyrosine hydroxylase-immunoreactive axons within the cerebral cortex. Axon densities and neuron densities were quantified using computer-assisted stereology. Prefrontal areas 9 and 32 were chosen for evaluation due to their roles in higher-order executive functions and theory of mind, respectively. Primary motor cortex (area 4) was also evaluated because it is not directly associated with cognition. We did not find an overt quantitative increase in cortical dopaminergic innervation in humans relative to the other primates examined. However, several differences in cortical dopaminergic innervation were observed among species which may have functional implications. Specifically, humans exhibited a sublaminar pattern of innervation in layer I of areas 9 and 32 that differed from that of macaques and chimpanzees. Analysis of axon length density to neuron density among species revealed that humans and chimpanzees together deviated from macaques in having increased dopaminergic afferents in layers III and V/VI of areas 9 and 32, but there were no phylogenetic differences in area 4. Finally, morphological specializations of axon coils that may be indicative of cortical plasticity events were observed in humans and chimpanzees, but not macaques. Our findings suggest significant modifications of dopamine's role in cortical organization occurred in the evolution of the apes, with further changes in the descent of humans.