Serena Bianchi

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

Neocortical development in humans is characterized by an extended period of synaptic proliferation that peaks in mid-childhood, with subsequent pruning through early adulthood, as well as relatively delayed maturation of neuronal arborization in the prefrontal cortex compared with sensorimotor areas. In macaque monkeys, cortical synaptogenesis peaks during early infancy and developmental changes in synapse density and dendritic spines occur synchronously across cortical regions. Thus, relatively prolonged synapse and neuronal maturation in humans might contribute to enhancement of social learning during development and transmission of cultural practices, including language. However, because macaques, which share a last common ancestor with humans ∼25 million years ago, have served as the predominant comparative primate model in neurodevelopmental research, the paucity of data from more closely related great apes leaves unresolved when these evolutionary changes in the timing of cortical development became established in the human lineage. To address this question, we used immunohistochemistry, electron microscopy, and Golgi staining to characterize synaptic density and dendritic morphology of pyramidal neurons in primary somatosensory (area 3b), primary motor (area 4), prestriate visual (area 18), and prefrontal (area 10) cortices of developing chimpanzees (Pan troglodytes). We found that synaptogenesis occurs synchronously across cortical areas, with a peak of synapse density during the juvenile period (3–5 y). Moreover, similar to findings in humans, dendrites of prefrontal pyramidal neurons developed later than sensorimotor areas. These results suggest that evolutionary changes to neocortical development promoting greater neuronal plasticity early in postnatal life preceded the divergence of the human and chimpanzee lineages.

Neuropil Distribution in the Cerebral Cortex Differs Between Humans and Chimpanzees

Increased connectivity of high‐order association regions in the neocortex has been proposed as a defining feature of human brain evolution. At present, however, there are limited comparative data to examine this claim fully. We tested the hypothesis that the distribution of neuropil across areas of the neocortex of humans differs from that of one of our closest living relatives, the common chimpanzee. The neuropil provides a proxy measure of total connectivity within a local region because it is composed mostly of dendrites, axons, and synapses. Using image analysis techniques, we quantified the neuropil fraction from both hemispheres in six cytoarchitectonically defined regions including frontopolar cortex (area 10), Brocas area (area 45), frontoinsular cortex (area FI), primary motor cortex (area 4), primary auditory cortex (area 41/42), and the planum temporale (area 22). Our results demonstrate that humans exhibit a unique distribution of neuropil in the neocortex compared to chimpanzees. In particular, the human frontopolar cortex and the frontoinsular cortex had a significantly higher neuropil fraction than the other areas. In chimpanzees these prefrontal regions did not display significantly more neuropil, but the primary auditory cortex had a lower neuropil fraction than other areas. Our results support the conclusion that enhanced connectivity in the prefrontal cortex accompanied the evolution of the human brain. These species differences in neuropil distribution may offer insight into the neural basis of human cognition, reflecting enhancement of the integrative capacity of the prefrontal cortex. J. Comp. Neurol. 520:2917–2929, 2012.

Neocortical neuron morphology in Afrotheria: comparing the rock hyrax with the African elephant

The mammalian neocortex contains a great variety of neuronal types. In particular, recent studies have shown substantial morphological diversity among spiny projecting neurons in species that diverged close to the base of the mammalian radiation (e.g., monotremes, afrotherians, and xenarthrans). Here, we used a Golgi technique to examine different neuronal morphologies in an afrotherian species, the rock hyrax (Procavia capensis), and provide a comparison with the related African elephant (Loxodonta africana). Results showed that spiny neurons in the rock hyrax neocortex exhibit less morphological variation than in elephants, displaying a higher frequency of relatively “typical” pyramidal neurons. A quantitative comparison of rock hyrax pyramidal neuron morphology between frontal and visual areas, moreover, revealed greater spine density of neurons in frontal cortex, but no differences in other morphological aspects. Regional variations in pyramidal structure have also been observed in the African elephant, as well as a number of primate species.

Neocortical grey matter distribution underlying voluntary, flexible vocalizations in chimpanzees.

Vocal learning is a key property of spoken language, which might also be present in nonhuman primate species, such as chimpanzees (Pan troglodytes), to a limited degree. While understanding the origins of vocal learning in the primate brain may help shed light on the evolution of speech and language, little is still known regarding the neurobiological correlates of vocal flexibility in nonhuman primates. The current study used voxel-based morphometry (VBM) to assess whether the cerebral cortex of captive chimpanzees that learned to voluntarily produce sounds to attract the attention of a human experimenter (attention-getting sounds) differs in grey matter distribution compared to chimpanzees that do not exhibit this behavior. It was found that chimpanzees that produce attention-getting sounds were characterized by increased grey matter in the ventrolateral prefrontal and dorsal premotor cortices. These findings suggest that the evolution of the capacity to flexibly modulate vocal output may be associated with reorganization of regions for motor control, including orofacial movements, in the primate brain.

Pattern and process in hominin brain size evolution are scale-dependent

A large brain is a defining feature of modern humans, yet there is no consensus regarding the patterns, rates and processes involved in hominin brain size evolution. We use a reliable proxy for brain size in fossils, endocranial volume (ECV), to better understand how brain size evolved at both clade- and lineage-level scales. For the hominin clade overall, the dominant signal is consistent with a gradual increase in brain size. This gradual trend appears to have been generated primarily by processes operating within hypothesized lineages—64% or 88% depending on whether one uses a more or less speciose taxonomy, respectively. These processes were supplemented by the appearance in the fossil record of larger-brained Homo species and the subsequent disappearance of smaller-brained Australopithecus and Paranthropus taxa. When the estimated rate of within-lineage ECV increase is compared to an exponential model that operationalizes generation-scale evolutionary processes, it suggests that the observed data were the result of episodes of directional selection interspersed with periods of stasis and/or drift; all of this occurs on too fine a timescale to be resolved by the current human fossil record, thus producing apparent gradual trends within lineages. Our findings provide a quantitative basis for developing and testing scale-explicit hypotheses about the factors that led brain size to increase during hominin evolution.