Abstract

Areas 44 and 45 have been identified in non-human primates as homologs of the human Broca region. Distribution of large and smaller pyramids and the ventro-lateral localization in the posterior frontal lobe enable their identification in non-human primates. Since only humans hold the ability of language, it has been hypothesized that differences in microstructure may, together with other anatomical factors, e.g., white matter tract connectivity, volumes of cortical areas and their molecular differentiation, be responsible for the lack (non-human primates) or ability (humans) of language. We sought to identify microstructural differences, by quantitatively studying the cytoarchitecture of areas 44 and 45 using layer-specific grey level indices (volume proportion of neuropil and cell bodies) in serially sectioned and cell body stained human, bonobo, chimpanzee, gorilla, orangutan and Macaca fascicularis brains. The main results are the interspecies differences in neuropil volume relative to cell bodies in all layers of both areas which allows a grouping of the different species into three major groups: Homo sapiens has the largest, great apes a markedly lower, and macaque the lowest neuropil volume. This indicates considerably more space for local and interregional connectivity in human brains, which matches recent studies of fiber tracts and spacing of cortical minicolumns because increasing connectivity also requires more space for axons and dendrites in the neuropil. The evolutionary enlargement of neuropil is, therefore, a major structural difference between humans and non-human primates which may correspond to the underlying functional differences.

Highlights

  • A comparison of language properties, e.g., syntactic abilities, recursive structure, between human, apes and macaques shows differences indicative of a considerable evolution in the human lineage (Fitch, 2011, 2018; Fitch, Huber, & Bugnyar, 2010; Friederici, 2017a, b; Friederici, Bahlmann, Heim, Schubotz, & Anwander, 2006a; Hauser, Chomsky, & Fitch, 2002, 2014)

  • Various studies were published on the architectonic properties of cortical areas in the inferior frontal region of non-human primate brains, which are thought to be the homologs of the Broca region in the human brain

  • Areas 44 and 45 could be identified by the same criteria across all ape brains (Figs. 4e8) and the macaque (Fig. 9). The cytoarchitecture of both areas was quantitatively analyzed in each species using the method of gray level index (GLI) measurement vertical to the cortical surface across all layers

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Summary

Introduction

A comparison of language properties, e.g., syntactic abilities, recursive structure, between human, apes and macaques shows differences indicative of a considerable evolution in the human lineage (Fitch, 2011, 2018; Fitch, Huber, & Bugnyar, 2010; Friederici, 2017a, b; Friederici, Bahlmann, Heim, Schubotz, & Anwander, 2006a; Hauser, Chomsky, & Fitch, 2002, 2014). The FOXP2 transcription factor in apes and monkeys are currently central to genetic analysis of language function (Konopka et al, 2012; Staes et al, 2017), since the amino acid coding and pattern of nucleotide polymorphism in the human FOXP2 gene compared to that of chimpanzee suggest an important role in human language evolution (Enard et al, 2002). Various studies were published on the architectonic properties of cortical areas in the inferior frontal region of non-human primate brains, which are thought to be the homologs of the Broca region in the human brain. A resting state study using PET (Rilling et al, 2007) suggests that chimpanzee brains differ from human brains by a lower activity in left-sided areas homolog to those which are involved in language processing in humans. At least the Broca homolog regions in chimpanzees are putatively involved in vocal signaling in the common ancestor of both humans and chimpanzees

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