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

Abstract

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.

Keywords: Golgi stain; brain; evolution; ontogeny.

Fig. 1.

(A) Individual cubic polynomial regression curves fit to counts of synaptophysin-immunoreactive puncta densities for areas 3b, 4, 18, and 10. (B) Photomicrograph of synaptophysin-immunoreactive puncta from the prefrontal cortex of an 11-y-old chimpanzee. (Scale bar, 25 μm.)

Fig. 2.

(A) Photomicrograph of synapses as observed under EM. Arrows indicate synaptic junctions. (Scale bar, 0.5 μm.) (B) Bivariate plot between synaptophysin-immunoreactive puncta densities and synaptic densities from EM data. Squares represent age 0, triangles age 2, diamonds age 6, and circles age 11. Color scheme for areas as in Fig. 1.

Fig. 3.

(A) Tracings of Golgi-stained pyramidal neurons in cortical areas 3b, 4, 18, and 10 in infant and adult chimpanzees. (Scale bar, 100 μm.) Below the tracing, close-up photomicrographs depict dendritic shafts of pyramidal neurons in (B) area 10 of a 1-y-old chimpanzee, (C) area 10 of an adult chimpanzee, (D) area 3b of a 1-y-old chimpanzee, and (E) area 3b of an adult chimpanzee. (Scale bar, 25 μm.)

Fig. 4.

Regional differences in morphological measures of complexity of basilar dendrites for all cortical regions of interest between adult and infant chimpanzees, including TDL, MSL, DSC, DSN, and DSD. Data from juveniles (5–9 y), for which one individual per age group was available, are illustrated as individual data points. Error bars represent SEM.