A Specialized Neural Circuit Gates Social Vocalizations in the Mouse

Tschida, Katherine; Michael, Valerie; Takatoh, Jun; Han, Bao-Xia; Zhao, Shengli; Sakurai, K.; Mooney, Richard; Wang, Fan

doi:10.1016/j.neuron.2019.05.025

Cited by 135 publications

(191 citation statements)

References 78 publications

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“…We find that periaqueductal gray neurons innervated by prelimbic cortex strongly project to brainstem nuclei involved in vocal pattern generation such as the intermediate reticular formation (Hage & Jürgens, ; Jürgens & Hage, ) and the nucleus retroambiguus (Holstege, ). A recent study supports the idea that periaqueductal gray neurons projecting to the brainstem gate vocalizations (Tschida et al., ). The viral transsynaptic labeling approach developed by Zingg et al.…”

Section: Discussionsupporting

confidence: 64%

Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control

Bennett

Maier

Brecht

2019

Eur J of Neuroscience

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Microstimulation mapping identified vocalization areas in primate anterior cingulate cortex. Rat anterior cingulate and medial prefrontal areas have also been intensely investigated, but we do not know, how these cortical areas contribute to vocalizations and no systematic mapping of stimulation‐evoked vocalizations has been performed. To address this question, we mapped microstimulation‐evoked (ultrasonic) vocalizations in rat cingulate and medial prefrontal cortex. The incidence of evoked vocalizations differed markedly between frontal cortical areas. Vocalizations were most often evoked in posterior prelimbic cortex and cingulate area 2, whereas vocalizations were rarely evoked in dorsal areas (vibrissa motor cortex, secondary motor cortex and cingulate area 1) and anterior areas (anterior prelimbic, medial‐/ventral‐orbital cortex). Vocalizations were observed at intermediate frequencies in ventro‐medial areas (infralimbic and dorsopeduncular cortex). Various complete, naturally occurring calls could be elicited. In prelimbic cortex superficial layer microstimulation evoked mainly fear calls with low efficacy, whereas deep layer microstimulation evoked mainly 50 kHz calls with high efficacy. Vocalization stimulation thresholds were substantial (70–500 μA, the maximum tested; on average ~400 μA) and latencies were long (median 175 ms). Posterior prelimbic cortex projected to numerous targets and innervated brainstem vocalization centers such as the intermediate reticular formation and the nucleus retroambiguus disynaptically via the periaqueductal gray. Anatomical position, stimulation effects and projection targets of posterior prelimbic cortex were similar to that of monkey anterior cingulate vocalization cortex. Our data suggest that posterior prelimbic cortex is more closely involved in control of vocalization initiation than in specifying acoustic details of vocalizations.

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Section: Discussionsupporting

confidence: 64%

Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control

Bennett

Maier

Brecht

2019

Eur J of Neuroscience

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“…We found that mouse listeners preferentially approached intact over irregular courtship songs, suggesting that regularity is attractive to females in the context of vocal-based mate selection. The temporal regularity observed in mouse songs is a consequence of breathing patterns regulating the production of syllables by the emitter, as individual calls are generated following the onset of exhalation 23,25,42 . Disruption to the temporal regularity of male song, as artificially introduced in this study, may for instance result from irregular breathing cycles and thus "stuttering" singing by the male, or by the inability to sustain bouts of vocal production of sufficient duration to elicit a salient percept of regularity in the listener.…”

Section: Discussionmentioning

confidence: 99%

“…The vocal patterns emitted in this context consisted of sequences of individual frequency-modulated calls (see example Fig. 1A, 3A, S1A and 3,9,[23][24][25]. Across the set of recorded male vocalizations, the duration of continuous call elements, or syllables, followed a bimodal distribution, with a majority of short syllables (local maximum = 23ms, 86% (2039/2373) of recorded syllables with durations shorter than 63ms (local minimum)) and a minority of long syllables (local maximum = 88 ms, 14%…”

Section: Acoustic Characteristics Of Vocal Sequences Emitted By Male mentioning

confidence: 99%

Courtship behaviour reveals temporal regularity is a critical social cue in mouse communication

Perrodin

Verzat

Bendor

2020

Preprint

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While animals navigating the real world face a barrage of complex sensory input, their brains have evolved to perceptually compress multidimensional information by selectively extracting the features relevant for survival. For instance, communication signals supporting social interactions in several mammalian species consist of acoustically complex sequences of vocalizations, however little is known about what information listeners extract from such timevarying sensory streams. Here, we utilize female mice's natural behavioural response to male courtship songs to evaluate the relevant acoustic dimensions used in their social decisions. We found that females were highly sensitive to disruptions of song temporal regularity, and preferentially approached playbacks of intact male songs over rhythmically irregular versions of the songs. In contrast, female behaviour was invariant to manipulations affecting the songs' sequential organization, or the spectrotemporal structure of individual syllables. The results reveal temporal regularity as a key acoustic cue extracted by mammalian listeners from complex vocal sequences during goal-directed social behaviour.

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“…Anatomical and physiological studies revealed that nRA neurons receive inputs from a variety of respiratory and vocal nuclei, including the Bötzinger and pre‐Bötzinger complexes, the PB complex, and the PAG. Neurons in nRA send direct projections to laryngeal and pharyngeal motor pools, and appear to serve as the “final common pathway” for vocal production in mammals (Holstege, 1989; Tschida et al., 2019). In cats, activating some parts of nRAinduced vocalizations, but did not change inspiration; stimulation in other areas of nRA did not induce vocal output, but instead increased respiration rates by shortening both inspiratory and expiratory phases (Subramanian & Holstege, 2009).…”

Section: Central Control Of Vocalization: Hindbrain Vocal Central Patmentioning

confidence: 99%

Inspiring song: The role of respiratory circuitry in the evolution of vertebrate vocal behavior

Barkan

Zornik

2020

Developmental Neurobiology

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Vocalization is a common means of communication across vertebrates, but the evolutionary origins of the neural circuits controlling these behaviors are not clear. Peripheral mechanisms of sound production vary widely: fish produce sounds with a swimbladder or pectoral fins; amphibians, reptiles, and mammalians vocalize using a larynx; birds vocalize with a syrinx. Despite the diversity of vocal effectors across taxa, there are many similarities in the neural circuits underlying the control of these organs. Do similarities in vocal circuit structure and function indicate that vocal behaviors first arose in a single common ancestor, or have similar neural circuits arisen independently multiple times during evolution? In this review, we describe the hindbrain circuits that are involved in vocal production across vertebrates. Given that vocalization depends on respiration in most tetrapods, it is not surprising that vocal and respiratory hindbrain circuits across distantly related species are anatomically intermingled and functionally linked. Such vocal‐respiratory circuit integration supports the hypothesis that vocal evolution involved the expansion and functional diversification of breathing circuits. Recent phylogenetic analyses, however, suggest vocal behaviors arose independently in all major tetrapod clades, indicating that similarities in vocal control circuits are the result of repeated co‐options of respiratory circuits in each lineage. It is currently unknown whether vocal circuits across taxa are made up of homologous neurons, or whether vocal neurons in each lineage arose from developmentally and evolutionarily distinct progenitors. Integrative comparative studies of vocal neurons across brain regions and taxa will be required to distinguish between these two scenarios.

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A Specialized Neural Circuit Gates Social Vocalizations in the Mouse

Cited by 135 publications

References 78 publications

Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control

Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control

Courtship behaviour reveals temporal regularity is a critical social cue in mouse communication

Inspiring song: The role of respiratory circuitry in the evolution of vertebrate vocal behavior

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