Midline section of the medulla abolishes inspiratory activity and desynchronizes pre-inspiratory neuron rhythm on both sides of the medulla in newborn rats

Onimaru, Hiroshi; Tsuzawa, Kayo; Nakazono, Yoshimi; Janczewski, Wiktor A.

doi:10.1152/jn.00554.2014

Cited by 6 publications

(6 citation statements)

References 37 publications

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“…They propose that each phase of the respiratory rhythm is generated by its own excitatory microcircuit located in a different region of the ventral respiratory group, the inspiratory phase being generated by the preBötC, postinspiration by its own complex (the PiCo) (Anderson et al 2016), and active expiration by the so-called lateral parafacial/ retrotrapezoidal group (Huckstepp et al 2016;Janczewski and Feldman 2006;Onimaru et al 2009). This idea is similar in spirit to the microcircuit models of Smith et al (2013), Molkov et al (2013), Koizumi et al (2013), andOnimaru et al (2015), which contain more areas. However, each of these excitatory microcircuits contains neurons with different anatomical, physiological, and modulatory properties, and each is dependent on excitatory synaptic transmission, able to generate rhythmicity in the absence of synaptic inhibition (Ramirez et al 2016).…”

Section: Discussionmentioning

confidence: 94%

“…To generate more than one phase, it is necessary to assemble a network in which excitatory microcircuits are segmented, via inhibition, into different compartments. Mutually inhibitory circuits have been proposed for the inspiration-active expiration network (Koizumi et al 2013;Molkov et al 2013;Onimaru et al 2015;Smith et al 2013) and preBötC-postinspiratory complex (PiCo) networks (Anderson et al 2016).…”

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confidence: 99%

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Different roles for inhibition in the rhythm-generating respiratory network

Harris

Dashevskiy²,

Mendoza³

et al. 2017

Journal of Neurophysiology

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Unraveling the interplay of excitation and inhibition within rhythm-generating networks remains a fundamental issue in neuroscience. We use a biophysical model to investigate the different roles of local and long-range inhibition in the respiratory network, a key component of which is the pre-Bötzinger complex inspiratory microcircuit. Increasing inhibition within the microcircuit results in a limited number of out-of-phase neurons before rhythmicity and synchrony degenerate. Thus unstructured local inhibition is destabilizing and cannot support the generation of more than one rhythm. A two-phase rhythm requires restructuring the network into two microcircuits coupled by long-range inhibition in the manner of a half-center. In this context, inhibition leads to greater stability of the two out-of-phase rhythms. We support our computational results with in vitro recordings from mouse pre-Bötzinger complex. Partial excitation block leads to increased rhythmic variability, but this recovers after blockade of inhibition. Our results support the idea that local inhibition in the pre-Bötzinger complex is present to allow for descending control of synchrony or robustness to adverse conditions like hypoxia. We conclude that the balance of inhibition and excitation determines the stability of rhythmogenesis, but with opposite roles within and between areas. These different inhibitory roles may apply to a variety of rhythmic behaviors that emerge in widespread pattern-generating circuits of the nervous system. The roles of inhibition within the pre-Bötzinger complex (preBötC) are a matter of debate. Using a combination of modeling and experiment, we demonstrate that inhibition affects synchrony, period variability, and overall frequency of the preBötC and coupled rhythmogenic networks. This work expands our understanding of ubiquitous motor and cognitive oscillatory networks.

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Section: Discussionmentioning

confidence: 94%

mentioning

confidence: 99%

Different roles for inhibition in the rhythm-generating respiratory network

Harris

Dashevskiy²,

Mendoza³

et al. 2017

Journal of Neurophysiology

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“…Valle & Beltran-Parrazal, 2017; lateral zone of , the parafacial respiratory group (see Onimaru et al, 2015) and/or Kölliker-Fuse nucleus (see Dutschmann et al, 2007) might distribute exclusively to respiratory-related motor outputs residing within the brainstem. Alternately, pre-inspiratory activity might distribute commonly to respiratory-related motor outputs above and below the level of the medullocervical confluence, with dedicated pathways presynaptically gating expression of pre-inspiratory activity in inspiratory-related spinal motor outputs tonically (see Song, Li, & Shao, 2000) and respiratory-related brainstem motor outputs state-dependently (see Lee et al, 2003).…”

Section: Parenteral Administration Of Fentanyl Attenuates Discharge Imentioning

confidence: 99%

“…Mechanical transection through rostral zones of the Bötzinger complex, retaining integrity of the retrotrapezoid nucleus and parafacial respiratory group, transiently abolishes the discharge in neurogram recordings of the facial nerve and ventral rootlets emanating from C4 segments of the cervical spinal cord, with interval recovery of the latter and persistent silence of the former (Onimaru et al., 2006: figure 5B). Midline sectioning through the medulla in brainstem–spinal cord preparations eliminates phasic discharge within C4 ventral rootlets and hypoglossal neural efferent activity and decouples pre‐inspiratory activity generated by neurons residing within the medulla (Onimaru, Tsuzawa, Nakazono, & Janczewski, 2015). These data suggest that any influence by propriobulbar interneuronal microcircuit oscillators exhibiting pre‐inspiratory discharge residing within the retrotrapezoid nucleus and lateral zone of the parafacial respiratory group upon facial motor output must be indirect, through the preBötzC.…”

Section: Propriobulbar Interneuronal Microcircuit Oscillators Conveyimentioning

confidence: 99%

Retracted: Control of hypoglossal pre‐inspiratory discharge

Ghali

2020

Experimental Physiology

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The hypoglossal nerve (XII) innervates muscles mediating excursive movements of the tongue. The population discharge of hypoglossalmotoneuronal axons constituting the hypoglossal nerve precedes and extends through the inspiratory epoch. The epoch subtended between the onsets of hypoglossal and phrenic neural discharge constitutes so-called pre-inspiration. Hypoglossal pre-inspiratory neural discharge serendipitously displaces the tongue along a tensor reducing upper airway resistance anticipative of succeeding inspiratory efforts. Hypoglossal motoneurons exhibiting discharge onset during pre-inspiration experience successive hyperpolarization of membrane voltage and attenuation of unitary spiking frequency, although a subset may, paradoxically and state-dependently, exhibit depolarization of membrane voltage and augmentation of neuronal spiking frequency, by dynamic stretch placed upon the alveolar walls and interstitium. Marked static elevation of positive-end expiratory pressure may induce hypoglossal bursting decoupled from phasic rhythmic phrenic discharge. Augmentation of the amplitude and/or duration of hypoglossal inspiratory discharge during successive pre-inspiratory and inspiratory epochs by inhalation of a hypoxic and/or hypercapnic gas mixture remains restrained in the presence of intact vagal inputs and is potentiated by interruptions of vagal continuity. Unravelling the mechanisms underlying the genesis of pre-inspiratory activity will inform our understanding of respiratory rhythm generation and pattern shaping. In the present work, I seek to explore the mechanisms underlying modulation of hypoglossal pre-inspiratory discharge by hypercapnia, hypoxia and static and dynamic lung stretch placed upon hypoglossal pre-inspiratory activity, the mechanisms underlying the generation of hypoglossal pre-inspiratory activity, and the extent of microanatomical and functional overlap between propriobulbar interneuronal microcircuits generating hypoglossal pre-inspiratory activity and propriobulbar interneuronal microcircuit oscillators generating pre-inspiratory activity inaugurally inducing respiratory rhythmic activity and thus use experimental data from previous work and that developed by other investigators to explore the modulatory role of lung vagal afferents and intra-neuraxial and carotid body chemoreceptors upon hypoglossal pre-inspiratory activity.

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“…In lampreys, basal vertebrates that do not vocalize, a rhythmically active anterior hindbrain nucleus (the pTRG) that projects to NA motor neurons drives fast inspiration (Cinelli et al, 2013) and is a likely parabrachial homolog. A second component of the lamprey respiratory CPG drives slow inspiration and is found in anterior NA (Missaghi et al, 2016) where the mammalian pre-inspiratory complex is located (Baertsch et al, 2018) and where midline transections abolish inspiration (Onimaru et al, 2015). Thus the Xenopus slow trill vocal CPG might also be found in anterior NA.…”

Section: Challenges: Vertebrate Vocal Circuitrymentioning

confidence: 99%

Generation, Coordination, and Evolution of Neural Circuits for Vocal Communication

et al. 2020

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In many species, vocal communication is essential for coordinating social behaviors including courtship, mating, parenting, rivalry, and alarm signaling. Effective communication requires accurate production, detection, and classification of signals, as well as selection of socially appropriate responses. Understanding how signals are generated and how acoustic signals are perceived is key to understanding the neurobiology of social behaviors. Here we review our long-standing research program focused on Xenopus, a frog genus which has provided valuable insights into the mechanisms and evolution of vertebrate social behaviors. In Xenopus laevis, vocal signals differ between the sexes, through development, and across the genus, reflecting evolutionary divergence in sensory and motor circuits that can be interrogated mechanistically. Using two ex vivo preparations, the isolated brain and vocal organ, we have identified essential components of the vocal production system: the sexually differentiated larynx at the periphery, and the hindbrain vocal central pattern generator (CPG) centrally, that produce sex-and species-characteristic sound pulse frequencies and temporal patterns, respectively. Within the hindbrain, we have described how intrinsic membrane properties of neurons in the vocal CPG generate species-specific vocal patterns, how vocal nuclei are connected to generate vocal patterns, as well as the roles of neurotransmitters and neuromodulators in activating the circuit. For sensorimotor integration, we identified a key forebrain node that links auditory and vocal production circuits to match socially appropriate vocal responses to acoustic features of male and female calls. The availability of a well supported phylogeny as well as reference genomes from several species now support analysis of the genetic architecture and the evolutionary divergence of neural circuits for vocal communication. Xenopus thus provides a vertebrate model in which to study vocal communication at many levels, from physiology, to behavior, and from development to evolution. As one of the most comprehensively studied phylogenetic groups within vertebrate vocal communication systems, Xenopus provides insights that can inform social communication across phyla.

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Midline section of the medulla abolishes inspiratory activity and desynchronizes pre-inspiratory neuron rhythm on both sides of the medulla in newborn rats

Cited by 6 publications

References 37 publications

Different roles for inhibition in the rhythm-generating respiratory network

Different roles for inhibition in the rhythm-generating respiratory network

Retracted: Control of hypoglossal pre‐inspiratory discharge

Generation, Coordination, and Evolution of Neural Circuits for Vocal Communication

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