Distinct Parietal and Temporal Pathways to the Homologues of Broca's Area in the Monkey

Abstract

An unprecedented detailed analysis of ventrolateral frontal cortical circuitry in Broca's area of the non-human primate brain clarifies the functional pathways permitting interaction between posterior cortical areas and the anterior language zone, providing important clues about the evolution of language. The homologues of the two distinct architectonic areas 44 and 45 that constitute the anterior language zone (Broca's region) in the human ventrolateral frontal lobe were recently established in the macaque monkey. Although we know that the inferior parietal lobule and the lateral temporal cortical region project to the ventrolateral frontal cortex, we do not know which of the several cortical areas found in those regions project to the homologues of Broca's region in the macaque monkey and by means of which white matter pathways. We have used the autoradiographic method, which permits the establishment of the cortical area from which axons originate (i.e., the site of injection), the precise course of the axons in the white matter, and their termination within particular cortical areas, to examine the parietal and temporal connections to area 44 and the two subdivisions of area 45 (i.e., areas 45A and 45B). The results demonstrated a ventral temporo-frontal stream of fibers that originate from various auditory, multisensory, and visual association cortical areas in the intermediate superolateral temporal region. These axons course via the extreme capsule and target most strongly area 45 with a more modest termination in area 44. By contrast, a dorsal stream of axons that originate from various cortical areas in the inferior parietal lobule and the adjacent caudal superior temporal sulcus was found to target both areas 44 and 45. These axons course in the superior longitudinal fasciculus, with some axons originating from the ventral inferior parietal lobule and the adjacent superior temporal sulcus arching and forming a simple arcuate fasciculus. The cortex of the most rostral part of the inferior parietal lobule is preferentially linked with the ventral premotor cortex (ventral area 6) that controls the orofacial musculature. The cortex of the intermediate part of the inferior parietal lobule is linked with both areas 44 and 45. These findings demonstrate the posterior parietal and temporal connections of the ventrolateral frontal areas, which, in the left hemisphere of the human brain, were adapted for various aspects of language production. These precursor circuits that are found in the nonlinguistic, nonhuman, primate brain also exist in the human brain. The possible reasons why these areas were adapted for language use in the human brain are discussed. The results throw new light on the prelinguistic precursor circuitry of Broca's region and help understand functional interactions between Broca's ventrolateral frontal region and posterior parietal and temporal association areas. Author SummaryTwo distinct cortical areas in the frontal lobe of the human brain, known as Broca's region, are involved with language production. This region has also been shown to exist in nonhuman primates. In this study, we explored the precise neural connectivity of Broca's region in macaque monkeys using the autoradiographic method to achieve a level of detail impossible in the human brain. We identified two major streams of connections feeding into Broca's area: a ventral stream from the temporal region, which includes areas processing auditory, multisensory, and visual information and a dorsal stream originating from the inferior parietal lobule and the adjacent superior temporal sulcus. Our detailed connectivity analysis illuminates the pathways via which posterior cortical areas can interact functionally with Broca's region, in addition to contributing to an understanding of the evolution of language. We suggest that a fundamental function of Broca's region is to retrieve information in a controlled strategic way from posterior cortical regions and to translate this information into action. This fundamental function was adapted during evolution of the left hemisphere of the human brain to serve language.