Department of Anthropology, The George Washington University, Washington, DC 20052, USA.
Proc Natl Acad Sci U S A. 2013 Jun 18;110 Suppl 2(Suppl 2):10395-401. doi: 10.1073/pnas.1301224110. Epub 2013 Jun 10.
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.
人类新皮层的发育特点是突触增殖期较长，在儿童中期达到峰值，随后在成年早期进行修剪，以及前额叶皮层神经元树突分支的成熟相对延迟，而与感觉运动区相比。在猕猴中，皮质突触发生在婴儿早期达到峰值，并且突触密度和树突棘的发育变化在皮质区域中同步发生。因此，人类相对较长的突触和神经元成熟可能有助于增强发育过程中的社会学习和文化实践的传播，包括语言。然而，由于与人类有大约 2500 万年前的最后共同祖先的猕猴一直是神经发育研究中的主要比较灵长类模型，因此，来自更密切相关的大猿的数据稀少，使得这些皮质发育时间的进化变化在人类谱系中何时确立仍未解决。为了解决这个问题，我们使用免疫组织化学、电子显微镜和高尔基染色来描述发育中的黑猩猩（Pan troglodytes）的初级体感（区域 3b）、初级运动（区域 4）、前纹状视觉（区域 18）和前额叶（区域 10）皮质中锥体神经元的突触密度和树突形态。我们发现，突触发生在皮质区域中同步进行，在青少年期（3-5 岁）达到突触密度峰值。此外，与人类的发现相似，前额叶锥体神经元的树突发育晚于感觉运动区。这些结果表明，促进新生后生命早期更大神经元可塑性的新皮层发育的进化变化先于人类和黑猩猩谱系的分化。
