A novel reticular node in the brainstem synchronizes neonatal mouse crying with breathing

Wei, Xin; Collie, Matthew; Dempsey, Bowen; Fortin, Gilles; Yackle, Kevin

doi:10.1016/j.neuron.2021.12.014

Cited by 33 publications

(45 citation statements)

References 63 publications

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“…Although no study to our knowledge has measured respiratory rates or patterns during the production of different non-vocal behaviors in mouse pups, it is possible that movement-associated changes in respiration promote USV production. On the one hand, brainstem respiratory circuits (Del Negro et al, 2018; Dutschmann & Dick, 2012; Pagliardini et al, 2011; Yackle et al, 2017; Zuperku et al, 2017; Ikeda et al, 2017) might influence the activity of brainstem neurons known to be important for USV production in adults (Hartmann & Brecht, 2020; JuÈrgens, 2002; Tschida et al, 2019) and pups (Hernandez-Miranda et al, 2017; Wei et al, 2022). A related possibility is that neuronal circuits important for movement generation, some of which in turn contribute to movement-related changes in respiration (Eldridge et al, 1981; Gariépy et al, 2012), might act on brainstem vocal-respiratory circuits to promote pup USV production.…”

Section: Discussionmentioning

confidence: 99%

“…Finally, we note that if for any reason a pup is in a behavioral state that is favorable to USV production, movement-related increases in respiratory rates per se could lead to increased rates of USV production. Rodents produce USVs as they exhale (Roberts, 1972; Sirotin et al, 2014; Wei et al, 2022), and movement-related increases in the number of respiratory cycles per second would provide more opportunities for USV production to occur than when pups are at rest.…”

Section: Discussionmentioning

confidence: 99%

“…Meanwhile, the mean pitch of isolation USVs becomes less variable over early development (Grimsley et al, 2011; Liu et al, 2003), and the interval between consecutive USVs decreases (Castellucci et al, 2018; Grimsley et al, 2011; Liu et al, 2003; Yin et al, 2016). These developmental changes in the acoustic features of isolation USVs are thought to be driven by physiological changes that take place during the first two postnatal weeks, including changes to the larynx, lung capacity, and vocal-respiratory coordination (Dutschmann et al, 2014; Elwood & Keeling, 1982; Riede et al, 2020; Wei et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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Rates but not acoustic features of ultrasonic vocalizations are related to non-vocal behaviors in mouse pups

Pranic

Kornbrek

Yang

et al. 2022

Preprint

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Mouse pups produce ultrasonic vocalizations (USVs) in response to isolation from the nest (i.e., isolation USVs). Rates and acoustic features of isolation USVs change dramatically over the first two weeks of life, and there is also substantial variability in the rates and acoustic features of isolation USVs at a given postnatal age. The factors that contribute to within-age variability in isolation USVs remain largely unknown. Here, we explore the extent to which non-vocal behaviors of mouse pups relate to the within-age variability in rates and acoustic features of their USVs. We recorded non-vocal behaviors of isolated C57BL/6J mouse pups at four postnatal ages (postnatal days 5, 10, 15, and 20), measured rates of isolation USV production, and applied a combination of hand-picked acoustic feature measurements and an unsupervised machine learning-based vocal analysis method to examine USV acoustic features. When we considered different categories of non-vocal behavior, our analyses revealed that mice in all postnatal age groups produce higher rates of isolation USVs during active non-vocal behaviors than when lying still. Moreover, rates of isolation USVs are correlated with the intensity (i.e., magnitude) of non-vocal body and limb movements within a given trial. In contrast, USVs produced during different categories of non-vocal behaviors and during different intensities of non-vocal movement do not differ substantially in their acoustic features. Our findings suggest that levels of behavioral arousal contribute to within-age variability in rates, but not acoustic features, of mouse isolation USVs.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Rates but not acoustic features of ultrasonic vocalizations are related to non-vocal behaviors in mouse pups

Pranic

Kornbrek

Yang

et al. 2022

Preprint

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“…As discussed below, a vocal CPG that patterns mouse pup cries has recently been identified in the inferior reticular formation (Wei et al, 2022 ). In Xenopus , the parabrachial nucleus (PB) is a CPG for the male advertrisement call [reviewed in Kelley et al ( 2020 )].…”

Section: Central Pattern Generators and Vocalizationmentioning

confidence: 99%

Convergent and divergent neural circuit architectures that support acoustic communication

Kelley

2022

Front. Neural Circuits

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Vocal communication is used across extant vertebrates, is evolutionarily ancient, and been maintained, in many lineages. Here I review the neural circuit architectures that support intraspecific acoustic signaling in representative anuran, mammalian and avian species as well as two invertebrates, fruit flies and Hawaiian crickets. I focus on hindbrain motor control motifs and their ties to respiratory circuits, expression of receptors for gonadal steroids in motor, sensory, and limbic neurons as well as divergent modalities that evoke vocal responses. Hindbrain and limbic participants in acoustic communication are highly conserved, while forebrain participants have diverged between anurans and mammals, as well as songbirds and rodents. I discuss the roles of natural and sexual selection in driving speciation, as well as exaptation of circuit elements with ancestral roles in respiration, for producing sounds and driving rhythmic vocal features. Recent technical advances in whole brain fMRI across species will enable real time imaging of acoustic signaling partners, tying auditory perception to vocal production.

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“…Bifunctional muscles similarly switch their participation between different behaviors, such as abdominal muscles in bats that contribute to respiration and the generation of echolocation signals (Lancaster et al 1995). In other cases, rhythmic networks and behaviors are co-active, and coordinating their activity via switching neurons is functionally important (Stickford and Stickford 2014; Wei et al 2022). Disrupted coordination can lead to behavioral deficits such as aspirating food when swallowing (Barlow 2009; Yagi et al 2017).…”

Section: Introductionmentioning

confidence: 99%

Multiple Intrinsic Membrane Properties are Modulated in a Switch from Single to Dual-Network Activity

Snyder

Blitz

2022

Preprint

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Neural network flexibility extends to changes in neuronal participation between networks. This neuronal switching can include neurons moving between single- and dual-network activity. We previously identified an example in which bursting at a second frequency occurs due to modulation of intrinsic membrane properties instead of synaptic recruitment into a second network. However, the intrinsic properties that are modulated were not determined. Here, we use small networks in the Jonah crab (Cancer borealis) stomatogastric nervous system (STNS) to examine modulation of intrinsic properties underlying neuropeptide- (Gly1-SIFamide) elicited neuronal switching. The LPG neuron switches from exclusive participation in the fast pyloric (~1 Hz) network, due to electrical coupling, to dual-network activity which includes periodic escapes from the fast rhythm via intrinsically-generated oscillations at the slower gastric mill network frequency (~0.1 Hz). We isolated LPG from both networks using pharmacology and hyperpolarizing current injection. Gly1-SIFamide increased LPG intrinsic excitability and rebound from inhibition, and decreased spike frequency adaptation, which can all contribute to intrinsic bursting. Using ion substitution and channel blockers, we found that a hyperpolarization-activated current, a persistent sodium current, and a calcium or calcium-related current(s) appear to be primary contributors to Gly1-SIFamide-elicited LPG intrinsic bursting. However, this intrinsic bursting was more sensitive to blocking currents when LPG received rhythmic electrical coupling input from the fast network than in the isolated condition. Overall, a switch from single- to dual-network activity can involve modulation of multiple intrinsic properties, while synaptic input from a second network can shape the contributions of these properties.

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A novel reticular node in the brainstem synchronizes neonatal mouse crying with breathing

Cited by 33 publications

References 63 publications

Rates but not acoustic features of ultrasonic vocalizations are related to non-vocal behaviors in mouse pups

Rates but not acoustic features of ultrasonic vocalizations are related to non-vocal behaviors in mouse pups

Convergent and divergent neural circuit architectures that support acoustic communication

Multiple Intrinsic Membrane Properties are Modulated in a Switch from Single to Dual-Network Activity

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