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Inhibition within a premotor circuit controls the timing of vocal turn-taking in zebra finches.

ABSTRACT: Vocal turn-taking is a fundamental organizing principle of human conversation but the neural circuit mechanisms that structure coordinated vocal interactions are unknown. The ability to exchange vocalizations in an alternating fashion is also exhibited by other species, including zebra finches. With a combination of behavioral testing, electrophysiological recordings, and pharmacological manipulations we demonstrate that activity within a cortical premotor nucleus orchestrates the timing of calls in socially interacting zebra finches. Within this circuit, local inhibition precedes premotor neuron activation associated with calling. Blocking inhibition results in faster vocal responses as well as an impaired ability to flexibly avoid overlapping with a partner. These results support a working model in which premotor inhibition regulates context-dependent timing of vocalizations and enables the precise interleaving of vocal signals during turn-taking.

SUBMITTER: Benichov JI

PROVIDER: S-EPMC6954284 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:ObjectivesThe primary objective of the study was to examine the occurrence and temporal structure of vocal turn-taking during spontaneous interactions between mothers and their children with cochlear implants (CI) over the first year after cochlear implantation as compared with interactions between mothers and children with normal hearing (NH).DesignMothers' unstructured play sessions with children with CI (n = 12) were recorded at 2 time points, 3 months (mean age 18.3 months) and 9 months (mean age 27.5 months) post-CI. A separate control group of mothers with age-matched hearing children (n = 12) was recorded at the same 2 time points. Five types of events were coded: mother and child vocalizations, vocalizations including speech overlap, and between- and within-speaker pauses. We analyzed the proportion of child and mother vocalizations involved in turn-taking, the temporal structure of turn-taking, and the temporal reciprocity of turn-taking using proportions of simultaneous speech and the duration of between- and within-speaker pauses.ResultsThe CI group produced a significantly smaller proportion of vocalizations in turn-taking than the NH group at the first session; however, CI children's proportion of vocalizations in turn-taking increased over time. There was a significantly larger proportion of simultaneous speech in the CI compared with the NH group at the first session. The CI group produced longer between-speaker pauses as compared with those in the NH group at the first session with mothers decreasing the duration of between-speaker pauses over time. NH infants and mothers in both groups produced longer within- than between-speaker pauses but CI infants demonstrated the opposite pattern. In addition, the duration of mothers' between-speaker pauses (CI and NH) was predicted by the duration of the infants' between-speaker pauses.ConclusionsVocal turn-taking and timing in both members of the dyad, the mother and infant, were sensitive to the experiential effects of child hearing loss and remediation with CI. Child hearing status affected dyad-specific coordination in the timing of responses between mothers and their children.

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Inhibition within a premotor circuit controls the timing of vocal turn-taking in zebra finches.

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