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Abstract The genusMacacais an ideal model for investigating the biological basis of primate social behavior from an evolutionary perspective. A significant amount of behavioral diversity has been reported among the macaque species, but little is known about the neural substrates that support this variation. The present study compared neural cell density and serotonergic innervation of the amygdala among four macaque species using histological and immunohistochemical methods. The species examined included rhesus (Macaca mulatta), Japanese (M. fuscata), pigtailed (M. nemestrina), and moor macaques (M. maura). We anticipated that the more aggressive rhesus and Japanese macaques would have lower serotonergic innervation within the amygdala compared to the more affiliative pigtailed and moor macaques. In contrast to our prediction, pigtailed macaques had higher serotonergic innervation than Japanese and moor macaques in the basal and central amygdala nuclei when controlling for neuron density. Our analysis of neural cell populations revealed that Japanese macaques possess significantly higher neuron and glia densities relative to the other three species, however we observed no glia‐to‐neuron ratio differences among species. The results of this study revealed serotonergic innervation and cell density differences among closely related macaque species, which may play a role in modulating subtle differences in emotional processing and species‐typical social styles. 

The nucleus accumbens (NAc) is central to motivation and action, exhibiting one of the highest densities of neuropeptide Y (NPY) in the brain. Within the NAc, NPY plays a role in reward and is involved in emotional behavior and in increasing alcohol and drug addiction and fat intake. Here, we examined NPY innervation and neurons of the NAc in humans and other anthropoid primates in order to determine whether there are differences among these various species that would correspond to behavioral or life history variables. We quantified NPY-immunoreactive axons and neurons in the NAc of 13 primate species, including humans, great apes, and monkeys. Our data show that the human brain is unique among primates in having denser NPY innervation within the NAc, as measured by axon length density to neuron density, even after accounting for brain size. Combined with our previous finding of increased dopaminergic innervation in the same region, our results suggest that the neurochemical profile of the human NAc appears to have rendered our species uniquely susceptible to neurophysiological conditions such as addiction. The increase in NPY specific to the NAc may represent an adaptation that favors fat intake and contributes to an increased vulnerability to eating disorders, obesity, as well as alcohol and drug dependence. Along with our findings for dopamine, these deeply rooted structural attributes of the human brain are likely to have emerged early in the human clade, laying the groundwork for later brain expansion and the development of cognitive and behavioral specializations. 

The amygdala is a sensory integration center that plays an important role in emotional learning, behavior, and motivation. Cannabinoid signaling in the amygdala modulates aspects of anxiety, aggression, and fear in rodents via cannabinoid receptor 1, however little is known about cannabinoid signaling in the amygdala of humans and nonhuman primates. Primates are behaviorally diverse, with closely related species often displaying distinct social styles characterized by varying degrees of social tolerance and agonistic tendencies. Such behavioral differences are thought to be associated with neurochemical differences among species. Given what is known about the functional role of cannabinoid signaling in the amygdala, we tested whether relatively tolerant species, such as humans, bonobos, and marmosets, possess relatively higher cannabinoid receptor 1-immunoreactive (CB1R-ir) axon density in the basolateral amygdala. We used immunohistochemistry and stereological methods to compare CB1R-ir axon density among 47 primates representing nine species: humans (n=5), chimpanzees (n=6), bonobos (n=2), baboons (n=6), rhesus macaques (n=5), Japanese macaques (n=6), pigtail macaques (n=6), marmosets (n=5), and capuchins (n=6). The basolateral amygdala is comprised of the lateral, basal, and accessory basal nuclei. Stereological data for each nucleus was collected separately. After ruling out sex differences within each species, we used repeated measures ANOVA to evaluate species differences. The interaction (F16,76 = 5.061, p<.001) and main effects of species (F8,38 = 8.007, p<.001) and area (F2,76 = 59.616, p<.001) were all significant. However, the observedspecies differences did not support our hypothesis related to social tolerance nor did the data conform to a phylogenetic pattern. Instead, we found that while some closely related species differed from each other in a nucleus-dependent manner, some distantly related species shared unexpected similarities. Our results highlight the need for additional comparative work on the cannabinoid system from a molecular and genetic perspective. We discuss the implications of our observations with special focus on primate brain evolution and its connection to primate social style. 

Endogenous and exogenous cannabinoids signal through the cannabinoid 1 receptor (CB1R) to modulate various aspects of social behavior, including aggression and anxiety. In rodents and primates, CB1R expression in the basolateral amygdala is dense and cannabinoid signaling in this region has been reported to influence social behavior. Little is known about how endocannabinoid signaling in the amygdala contributes to primate social diversity. The behaviorally diverse and species-rich cercopithecoid monkey genus Macaca is an ideal model for addressing this topic. Japanese (Macaca fuscata) and rhesus macaques (M. mulatta) display similar social styles in some respects; however, there is evidence to suggest they differ in their stress response, amygdala structure, and monoaminergic signaling. To further assess the molecular basis of social style in Japanese and rhesus macaques, we used immunohistochemistry and stereological methods to compare CB1R-immunoreactive (CB1R-ir) axon density in the basolateral amygdala, which is comprised of the lateral, basal, and accessory basal nuclei. Our study sample included 6 Japanese and 5 rhesus macaques. Repeated-measures ANOVAs were used to evaluate species differences, with amygdala region as the within-subjects measure and species as the between-subjects factor. This revealed significant main effects for species and area (p values < 0.05) with no interaction. Post hoc tests revealed higher CB1R-ir axon density in the basal and accessory basal nuclei of rhesus macaques compared to Japanese macaques. Our results suggest that CB1R-mediated signaling in the lateral nucleus of the amygdala is comparable between the two species, while the differences we observed in the basal and accessory basal nuclei may contribute to the nuanced behavioral differences observed between them. 

Previously identified differences in serotonin innervation have been proposed to underlie differences in behavior, such as personality style and sociability. Contrasting serotonergic fiber densities have been found in the amygdala of chimpanzees versus bonobos, and humans and apes are known to have more serotonin than monkeys in the dorsal and medial caudate nucleus and dorsal putamen. Our present work builds on earlier results by examining serotonergic axon innervation density in the nucleus accumbens and ventral pallidum, two important nodes in the reward system. The present sample included humans (n = 6; NIH NeuroBioBank), pigtailed macaque monkeys (n = 5; National Primate Research Center, University of Washington), and capuchin monkeys (n = 6; Alpha Genesis). All individuals were adult and free of neuropathological alterations. Brain sections were immunohistochemically processed for serotonin transporter (SERT) (Millipore, MAB 5618), and stereological methods (SpaceBalls probe, MBF Bioscience) were used to quantify the length density of SERT-immunoreactive axons and neuron densities from adjacent Nissl-stained sections. Repeated measures ANOVA was used to evaluate differences of SERT-immunoreactive axon densities and neuron densities among species. The main effect of brain region was significant (F 1,2 = 12.25, p = 0.004) with greater SERT innervation in ventral pallidum compared to the nucleus accumbens in all species. The main effect of species and the interaction of species x brain region were not significant. Based on these results, the serotonergic system in the nucleus accumbens and ventral pallidum appears to be evolutionarily conserved in the amount of innervation supplied to neurons among human and other anthropoid primates.