Dendritic Morphology of Pyramidal Neurons in the Chimpanzee Neocortex: Regional Specializations and Comparison to Humans

Abstract

The primate cerebral cortex is characterized by regional variation in the structure of pyramidal neurons, with more complex dendritic arbors and greater spine density observed in prefrontal compared with sensory and motor cortices. Although there are several investigations in humans and other primates, virtually nothing is known about regional variation in the morphology of pyramidal neurons in the cerebral cortex of great apes, humans' closest living relatives. The current study uses the rapid Golgi stain to quantify the dendritic structure of layer III pyramidal neurons in 4 areas of the chimpanzee cerebral cortex: Primary somatosensory (area 3b), primary motor (area 4), prestriate visual (area 18), and prefrontal (area 10) cortex. Consistent with previous studies in humans and macaque monkeys, pyramidal neurons in the prefrontal cortex of chimpanzees exhibit greater dendritic complexity than those in other cortical regions, suggesting that prefrontal cortical evolution in primates is characterized by increased potential for integrative connectivity. Compared with chimpanzees, the pyramidal neurons of humans had significantly longer and more branched dendritic arbors in all cortical regions.

Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans

“…4. Pyramidal neurons of the prefrontal cortex continued to be the least elaborate among the cortical areas examined according to most measures of dendritic complexity through infancy and juvenile development (ages 5-6) and only began to increase in the later juvenile period (age 9), ultimately becoming the most complex neurons in adulthood (32).…”

“…In addition to synaptogenesis, we examined regional changes in the development of dendritic branching of pyramidal neurons. In adult primates, remarkable variation in the morphology and complexity of pyramidal neurons has been reported (20,31,32,39). Specifically, it has been shown that pyramidal neurons of the prefrontal cortex are characterized by more elaborate dendritic trees than other cortical areas, to support increased connectivity from integrating diverse corticocortical inputs and to orchestrate cognitively complex behaviors (20,31,32,40).…”

“…In adult primates, remarkable variation in the morphology and complexity of pyramidal neurons has been reported (20,31,32,39). Specifically, it has been shown that pyramidal neurons of the prefrontal cortex are characterized by more elaborate dendritic trees than other cortical areas, to support increased connectivity from integrating diverse corticocortical inputs and to orchestrate cognitively complex behaviors (20,31,32,40). Although dendritic arbors are more extensive in the prefrontal cortex relative to other cortical regions in adult humans (31), chimpanzees (32), and macaques (20), the timing of development of these neuronal specializations appears to be species-specific (13,14).…”

“…Data for comparisons with adult chimpanzees, as shown in Fig. 4, were taken from a previous study that used the same methodological procedure (32), and included seven individuals, age 35+ y.…”

“…Therefore, the present study examined two developmental markers in chimpanzees, synaptogenesis and dendritic growth of pyramidal neurons, in four regions, including prestriate visual (area 18), primary motor (area 4), primary somatosensory (area 3b), and prefrontal (area 10) cortices. Previous studies of neuron morphology in adult primates have shown that these areas form a functional hierarchy whereby association cortices (i.e., area 10) that integrate input from other areas display greater potential for corticocortical connectivity than unimodal, sensory and motor regions (area 4, 3b, and 18) (20,31,32). We predicted that, if chimpanzee cortical development is more similar to humans than to macaques, synaptogenesis and maturation of dendritic arbors of pyramidal neurons would be extended into the juvenile period, and show a more prolonged trajectory in the prefrontal cortex relative to other regions.…”