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Structural changes involving new neurons can occur through stem cell-driven neurogenesis, and through incorporation of late-maturing “immature” neurons into networks, namely undifferentiated neuronal precursors frozen in a state of arrested maturation. The latter have been found in the cerebral cortex and are particularly abundant in large-brained mammals, covarying with the size of the brain and cortex. Similar cells have been described in the amygdala of some species, although their features and interspecies variation remain poorly understood. Here, their occurrence, number, morphology, molecular expression, age-related changes, and anatomical distribution in amygdala subdivisions were systematically analyzed in eight diverse mammalian species (including mouse, naked mole rat, rabbit, marmoset, cat, sheep, horse, and chimpanzee) widely differing in neuroanatomy, brain size, life span, and socioecology. We identify converging evidence that these amygdala cells are immature neurons and show marked phylogenetic variation, with a significantly greater prevalence in primates. The immature cells are largely located within the amygdala’s basolateral complex, a region that has expanded in primate brain evolution in conjunction with cortical projections. In addition, amygdala immature neurons also appear to stabilize in number through adulthood and old age, unlike other forms of plasticity that undergo marked age-related reduction. These results support the emerging view that large brains performing complex socio-cognitive functions rely on wide reservoirs of immature neurons. 

ABSTRACT The nucleus accumbens (NAcc) and ventral pallidum (VP) are key nodes in the mesolimbic reward pathway that facilitate stimulus salience, including the regulation of social motivation and attachment. Primate species display variation in social behaviors, including different levels of impulsivity, bonding, and aggression. Previous research has implicated neuromodulation of the reward pathway in the differential expression of various social behaviors, suggesting that differences in neurotransmitter innervation may play a role in species‐specific patterns. To explore this, we examined serotonergic innervation in the NAcc and VP among primates. We used stereology to quantify serotonin transporter‐immunoreactive (SERT‐ir) axon length density in the NAcc and VP of 13 primate species, including humans, great apes, and cercopithecid and platyrrhine monkeys. Our data show that serotonergic innervation density within both the NAcc and VP is highly conserved among species. This finding contrasts with our previous findings of higher levels of SERT‐ir axons in the dorsal striatum of humans and great apes relative to monkeys, a human‐specific increase in dopaminergic innervation within the NAcc and VP, and a human‐specific increase of neuropeptide Y in the NAcc, highlighting the mosaic nature of innervation patterns among species. 

Abstract Neuronal plasticity can vary remarkably in its form and degree across animal species. Adult neurogenesis, namely the capacity to produce new neurons from neural stem cells through adulthood, appears widespread in non-mammalian vertebrates, whereas it is reduced in mammals. A growing body of comparative studies also report variation in the occurrence and activity of neural stem cell niches between mammals, with a general trend of reduction from small-brained to large-brained species. Conversely, recent studies have shown that large-brained mammals host large amounts of neurons expressing typical markers of neurogenesis in the absence of cell division. In layer II of the cerebral cortex, populations of prenatally generated, non-dividing neurons continue to express molecules indicative of immaturity throughout life (cortical immature neurons; cINs). After remaining in a dormant state for a very long time, these cINs retain the potential of differentiating into mature neurons that integrate within the preexisting neural circuits. They are restricted to the paleocortex in small-brained rodents, while extending into the widely expanded neocortex of highly gyrencephalic, large-brained species. The current hypothesis is that these populations of non-newly generated “immature” neurons might represent a reservoir of developmentally plastic cells for mammalian species that are characterized by reduced stem cell-driven adult neurogenesis. This indicates that there may be a trade-off between various forms of plasticity that coexist during brain evolution. This balance may be necessary to maintain a “reservoir of plasticity” in brain regions that have distinct roles in species-specific socioecological adaptations, such as the neocortex and olfactory structures. 

Abstract Human newborns are considered altricial compared with other primates because they are relatively underdeveloped at birth. However, in a broader comparative context, other mammals are more altricial than humans. It has been proposed that altricial development evolved secondarily in humans due to obstetrical or metabolic constraints, and in association with increased brain plasticity. To explore this association, we used comparative data from 140 placental mammals to measure how altriciality evolved in humans and other species. We also estimated how changes in brain size and gestation length influenced the timing of neurodevelopment during hominin evolution. Based on our data, humans show the highest evolutionary rate to become more altricial (measured as the proportion of adult brain size at birth) across all placental mammals, but this results primarily from the pronounced postnatal enlargement of brain size rather than neonatal changes. In addition, we show that only a small number of neurodevelopmental events were shifted to the postnatal period during hominin evolution, and that they were primarily related to the myelination of certain brain pathways. These results indicate that the perception of human altriciality is mostly driven by postnatal changes, and they point to a possible association between the timing of myelination and human neuroplasticity. 

Primate evolution has led to a remarkable diversity of behavioral specializations and pronounced brain size variation among species (Barton, 2012; DeCasien and Higham, 2019; Powell et al., 2017). Gene expression provides a promising opportunity for studying the molecular basis of brain evolution, but it has been explored in very few primate species to date (e.g. Khaitovich et al., 2005; Khrameeva et al., 2020; Ma et al., 2022; Somel et al., 2009). To understand the landscape of gene expression evolution across the primate lineage, we generated and analyzed RNA-seq data from four brain regions in an unprecedented eighteen species. Here, we show a remarkable level of variation in gene expression among hominid species, including humans and chimpanzees, despite their relatively recent divergence time from other primates. We found that individual genes display a wide range of expression dynamics across evolutionary time reflective of the diverse selection pressures acting on genes within primate brain tissue. Using our samples that represent a 190-fold difference in primate brain size, we identified genes with variation in expression most correlated with brain size. Our study extensively broadens the phylogenetic context of what is known about the molecular evolution of the brain across primates and identifies novel candidate genes for the study of genetic regulation of brain evolution. 

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.