title: 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.
authors.affiliation: Department of Anthropology, The George Washington University, Washington, DC 20052, USA. sbianchi@gwmail.gwu.edu
authors.forename: Serena
authors.initials: S
authors.lastname: Bianchi
authors.forename: Cheryl D
authors.initials: CD
authors.lastname: Stimpson
authors.forename: Tetyana
authors.initials: T
authors.lastname: Duka
authors.forename: Michael D
authors.initials: MD
authors.lastname: Larsen
authors.forename: William G M
authors.initials: WG
authors.lastname: Janssen
authors.forename: Zachary
authors.initials: Z
authors.lastname: Collins
authors.forename: Amy L
authors.initials: AL
authors.lastname: Bauernfeind
authors.forename: Steven J
authors.initials: SJ
authors.lastname: Schapiro
authors.forename: Wallace B
authors.initials: WB
authors.lastname: Baze
authors.forename: Mark J
authors.initials: MJ
authors.lastname: McArthur
authors.forename: William D
authors.initials: WD
authors.lastname: Hopkins
authors.forename: Derek E
authors.initials: DE
authors.lastname: Wildman
authors.forename: Leonard
authors.initials: L
authors.lastname: Lipovich
authors.forename: Christopher W
authors.initials: CW
authors.lastname: Kuzawa
authors.forename: Bob
authors.initials: B
authors.lastname: Jacobs
authors.forename: Patrick R
authors.initials: PR
authors.lastname: Hof
authors.forename: Chet C
authors.initials: CC
authors.lastname: Sherwood
mesh_terms: D000818:Animals; D003712:Dendrites / Q000502:physiology; D056228:Feedback, Sensory / Q000502:physiology; D005260:Female; D006801:Humans; D008297:Male; D019579:Neocortex / Q000166:cytology / Q000502:physiology; D002679:Pan troglodytes / Q000033:anatomy & histology / Q000502:physiology; D010802:Phylogeny; D017966:Pyramidal Cells / Q000166:cytology / Q000502:physiology; D013569:Synapses / Q000502:physiology*
keywords: Golgi stain; brain; evolution; ontogeny