Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

Michael, Valerie; Goffinet, Jack; Pearson, J. M.; Wang, Fan; Tschida, Katherine; Mooney, Richard

doi:10.7554/elife.63493

Cited by 62 publications

(108 citation statements)

References 86 publications

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“…5). These same features have been shown to contribute to motor pattern generation in both invertebrates and vertebrates [13,42,60,61,62,63,64,65,66,67], although they are combined in new ways within the male song circuit. Such a minimalist circuit design both offers a simple control mechanism that allows the male to react to rapid changes in sensory context, and requires only few developmental changes to either derive this circuit from a unisex template [30] or alter the circuit to generate new song types in other species [21].…”

Section: Discussionmentioning

confidence: 91%

Flexible Circuit Mechanisms for Context-Dependent Song Sequencing

Roemschied

et al. 2021

Preprint

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Many sequenced behaviors, including locomotion, reaching, and vocalization, are patterned differently in different contexts, enabling animals to adjust to their current environments. However, how contextual information shapes neural activity to flexibly alter the patterning of actions is not yet understood. Prior work indicates such flexibility could be achieved via parallel motor circuits, with differing sensitivities to sensory context [1, 2, 3]; instead we demonstrate here how a single neural pathway operates in two different regimes dependent on recent sensory history. We leverage the Drosophila song production system [4] to investigate the neural mechanisms that support male song sequence generation in two contexts: near versus far from the female. While previous studies identified several song production neurons[5, 6, 7, 8], how these neurons are organized to mediate song patterning was unknown. We find that male flies sing ‘simple’ trains of only one syllable or mode far from the female but complex song sequences consisting of alternations between modes when near to her. We characterize the male song circuit from the brain to the ventral nerve cord (VNC), and find that the VNC song pre-motor circuit is shaped by two key computations: mutual inhibition and rebound excitability [9] between nodes driving the two modes of song. Weak sensory input to a direct brain-to-VNC excitatory pathway (via pC2 brain and pIP10 descending neurons) drives simple song far from the female. Strong sensory input to the same pathway enables complex song production via simultaneous recruitment of P1a neuron-mediated disinhibition of the VNC song pre-motor circuit. Thus, proximity to the female effectively unlocks motor circuit dynamics in the correct sensory context. We construct a compact circuit model to demonstrate that these few computations are sufficient to replicate natural context-dependent song dynamics. These results have broad implications for neural population-level models of context-dependent behavior [10] and highlight that canonical circuit motifs [11, 12, 13] can be combined in novel ways to enable circuit flexibility required for dynamic communication.

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Section: Discussionmentioning

confidence: 91%

Flexible Circuit Mechanisms for Context-Dependent Song Sequencing

Roemschied

et al. 2021

Preprint

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“…Recent work revealed that estrogen receptor 1 (ESR1) -expressing neurons in the preoptic area and the ventromedial hypothalamus participate in mouse USV (Chen et al, 2021;Gao et al, 2019;Karigo et al, 2021;Michael et al, 2020). In addition, motor neuron pools in the brain stem and spinal cord that control laryngeal and respiratory muscles also contribute to vocalization in mammals (Arriaga et al, 2012;Jurgens, 2002;Jurgens and Hage, 2007).…”

Section: Expression Of Tcf7l2 In Vglu2-positive Neurons Is Sufficient and Necessary For Mouse Vocalizationmentioning

confidence: 99%

TCF7L2 acts as a molecular switch in midbrain to control mammal vocalization through a transcriptional repression mechanism

Luo

et al. 2022

Preprint

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Vocalization is an essential medium for sexual and social signaling in birds and mammals. Periaqueductal gray (PAG) a conserved midbrain structure is believed to be responsible for innate vocalizations, but its molecular regulation remains largely unknown. Here, through a mouse forward genetic screening we identified one of the key Wnt/β-catenin effectors TCF7L2/TCF4 controls ultrasonic vocalization (USV) production and syllable complexity during maternal deprivation and sexual encounter. Expression of TCF7L2 in PAG excitatory neurons is necessary for the complex trait, while TCF7L2 loss reduces neuronal gene expressions and synaptic transmission in PAG. TCF7L2-mediated vocal control is independent of its β-catenin-binding domain but dependent of its DNA binding ability. Patient mutations associated with severe speech delay disrupt the transcriptional repression effect of TCF7L2, while mice carrying those mutations display severe USV impairments. Therefore, we conclude that TCF7L2 orchestrates gene expression in midbrain to control vocal production through a transcriptional repression mechanism.

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“…While the neural circuit involved in USV production [ 69 , 152 , 153 , 154 ] and the correlates of USV perception in the brain of conspecific receivers [ 155 , 156 , 157 ] are well-documented, the effect of USV production on the sender animal’s brain activity has been largely overlooked. Yet, such information is needed to better understand how the different components of fear response collectively modulate a rat’s brain neural dynamics.…”

Section: Usv Emission Impacts Brain Activitymentioning

confidence: 99%

Ultrasonic Vocalizations Emission across Development in Rats: Coordination with Respiration and Impact on Brain Neural Dynamics

Boulanger-Bertolus

Mouly

2021

Brain Sciences

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Rats communicate using ultrasonic vocalizations (USV) throughout their life when confronted with emotionally stimulating situations, either negative or positive. The context of USV emission and the psychoacoustic characteristics of the vocalizations change greatly between infancy and adulthood. Importantly, the production of USV is tightly coordinated with respiration, and respiratory rhythm is known to influence brain activity and cognitive functions. This review goes through the acoustic characteristics and mechanisms of production of USV both in infant and adult rats and emphasizes the tight relationships that exist between USV emission and respiration throughout the rat’s development. It further describes how USV emission and respiration collectively affect brain oscillatory activities. We discuss the possible association of USV emission with emotional memory processes and point out several avenues of research on USV that are currently overlooked and could fill gaps in our knowledge.

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Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

Cited by 62 publications

References 86 publications

Flexible Circuit Mechanisms for Context-Dependent Song Sequencing

Flexible Circuit Mechanisms for Context-Dependent Song Sequencing

TCF7L2 acts as a molecular switch in midbrain to control mammal vocalization through a transcriptional repression mechanism

Ultrasonic Vocalizations Emission across Development in Rats: Coordination with Respiration and Impact on Brain Neural Dynamics

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