Dataset Information

Distinct neural networks for the volitional control of vocal and manual actions in the monkey homologue of Broca's area.

ABSTRACT: The ventrolateral frontal lobe (Broca's area) of the human brain is crucial in speech production. In macaques, neurons in the ventrolateral prefrontal cortex, the suggested monkey homologue of Broca's area, signal the volitional initiation of vocalizations. We explored whether this brain area became specialized for vocal initiation during primate evolution and trained macaques to alternate between a vocal and manual action in response to arbitrary cues. During task performance, single neurons recorded from the ventrolateral prefrontal cortex and the rostroventral premotor cortex of the inferior frontal cortex predominantly signaled the impending vocal or, to a lesser extent, manual action, but not both. Neuronal activity was specific for volitional action plans and differed during spontaneous movement preparations. This implies that the primate inferior frontal cortex controls the initiation of volitional utterances via a dedicated network of vocal selective neurons that might have been exploited during the evolution of Broca's area.

SUBMITTER: Gavrilov N

PROVIDER: S-EPMC7857725 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Distinct neural networks for the volitional control of vocal and manual actions in the monkey homologue of Broca's area.

Gavrilov Natalja N Nieder Andreas A

eLife 20210203

The ventrolateral frontal lobe (Broca's area) of the human brain is crucial in speech production. In macaques, neurons in the ventrolateral prefrontal cortex, the suggested monkey homologue of Broca's area, signal the volitional initiation of vocalizations. We explored whether this brain area became specialized for vocal initiation during primate evolution and trained macaques to alternate between a vocal and manual action in response to arbitrary cues. During task performance, single neurons re ...[more]

PMID: 33534697

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Project description: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.

Dataset Information

Distinct neural networks for the volitional control of vocal and manual actions in the monkey homologue of Broca's area.

Publications

Distinct neural networks for the volitional control of vocal and manual actions in the monkey homologue of Broca's area.

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