A V0 core neuronal circuit for inspiration

Wu, Jinjin; Capelli, Paolo; Bouvier, Julien; Goulding, Martyn; Arber, Silvia; Fortin, Gilles

doi:10.1038/s41467-017-00589-2

Cited by 54 publications

(72 citation statements)

References 67 publications

(88 reference statements)

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“…This organization may act to integrate activity of phrenic motoneurons during the respiratory cycle, as well as facilitate interactions between phrenic motoneurons and adjacent motoneurons responsible for controlling accessory respiratory muscles (Scheibel & Scheibel, , ). Afferent input from the brainstem has also been shown to follow the somatic and dendritic distribution of phrenic motoneurons (Ellenberger & Feldman, ; Ellenberger, Vera, Haselton, Haselton, & Schneiderman, ; Furicchia & Goshgarian, ; Wu et al, ).…”

Section: Discussionmentioning

confidence: 99%

Phrenic motoneuron structural plasticity across models of diaphragm muscle paralysis

Mantilla

Zhan

Gransee

et al. 2018

J of Comparative Neurology

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Structural plasticity in motoneurons may be influenced by activation history and motoneuron-muscle fiber interactions. The goal of this study was to examine morphological adaptations of phrenic motoneurons following imposed motoneuron inactivity while controlling for diaphragm muscle inactivity. Well-characterized rat models were used including unilateral C2 spinal hemisection (SH; ipsilateral phrenic motoneurons and diaphragm muscle are inactive) and tetrodotoxin phrenic nerve blockade (TTX; ipsilateral diaphragm muscle is paralyzed while phrenic motoneuron activity is preserved). We hypothesized that inactivity of phrenic motoneurons would result in a decrease in motoneuron size, consistent with a homeostatic increase in excitability. Phrenic motoneurons were retrogradely labeled by ipsilateral diaphragm muscle injection of fluorescent dextrans or cholera toxin subunit B. Following 2 weeks of diaphragm muscle paralysis, morphological parameters of labeled ipsilateral phrenic motoneurons were assessed quantitatively using fluorescence confocal microscopy. Compared to controls, phrenic motoneuron somal volumes and surface areas decreased with SH, but increased with TTX. Total phrenic motoneuron surface area was unchanged by SH, but increased with TTX. Dendritic surface area was estimated from primary dendrite diameter using a power equation obtained from 3D reconstructed phrenic motoneurons. Estimated dendritic surface area was not significantly different between control and SH, but increased with TTX. Similarly, TTX significantly increased total phrenic motoneuron surface area. These results suggest that ipsilateral phrenic motoneuron morphological adaptations are consistent with a normalization of motoneuron excitability following prolonged alterations in motoneuron activity. Phrenic motoneuron structural plasticity is likely more dependent on motoneuron activity (or descending input) than muscle fiber activity.

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Section: Discussionmentioning

confidence: 99%

Phrenic motoneuron structural plasticity across models of diaphragm muscle paralysis

Mantilla

Zhan

Gransee

et al. 2018

J of Comparative Neurology

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“…If Dbx1-derived expiratory neurons in the 343 Bötzinger complex exist (which has not been demonstrated), then their photostimulation would 344 depress breathing (Janczewski et al, 2013; Marchenko et al, 2016), the opposite of what we 345 measured. If photostimulation affected Dbx1 phrenic premotor neurons in the rostral ventral 346 respiratory group(Wu et al, 2017), then that would enhance the magnitude of inspiratory 347 breaths, but not the inspiratory timing circuits in the preBötC. Sustained photostimulation 348 experiments only enhanced breathing frequency and never VT, which diminishes the likelihood 349 that our protocols influenced Dbx1-derived phrenic premotoneurons.…”

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confidence: 91%

Dbx1 pre-Bötzinger complex interneurons comprise the core inspiratory oscillator for breathing in adult mice

Vann

et al. 2018

Preprint

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17The brainstem pre-Bötzinger complex (preBötC) generates inspiratory breathing rhythms, but 18 which neurons comprise its rhythmogenic core? Dbx1-derived neurons may play the preeminent 19 role in rhythm generation, an idea well founded at perinatal stages of development but not in 20 adulthood. We expressed archaerhodopsin or channelrhodopsin in Dbx1 preBötC neurons in 21 intact adult mice to interrogate their function. Prolonged photoinhibition slowed down or stopped 22 breathing, whereas prolonged photostimulation sped up breathing. Brief inspiratory-phase 23 photoinhibition evoked the next breath earlier than expected, whereas brief expiratory-phase 24 photoinhibition delayed the subsequent breath. Conversely, brief inspiratory-phase 25 photostimulation increased inspiratory duration and delayed the subsequent breath, whereas 26 brief expiratory-phase photostimulation evoked the next breath earlier than expected. Because 27 they govern the frequency and precise timing of breaths in awake adult mice with sensorimotor 28 feedback intact, Dbx1 preBötC neurons constitute an essential core component of the 29 inspiratory oscillator, knowledge directly relevant to human health and physiology. 30

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“…Efficient breathing, however, requires synchronous inspiration and expiration on the left and right sides. V0 neurons (most likely in the brainstem) are critical for this coordination because disruption of commissural projections of V0 neurons results in left-right desynchronized inspiration (and neonatal lethality; Wu et al, 2017). Thus, similar neural building blocks may be used in different ways in locomotor vs. respiratory circuits.…”

Section: Developmental Neuron Classes Perform Distinct Functionsmentioning

confidence: 99%

“…For example, Wu et al (2017) used a combination of viral tracing and transgenic labeling methods to show that brainstem neurons of the V0 class in the PBC and rVRG are critical components of the circuits driving inspiration. Moreover, they were able to disrupt the development of these neurons to demonstrate the importance of commissural projections for the synchronous activity of the left and right side of the diaphragm.…”

Section: Potential Roles For Developmental Neuron Classes In Breathingmentioning

confidence: 99%

Role of Propriospinal Neurons in Control of Respiratory Muscles and Recovery of Breathing Following Injury

Jensen

Alilain

Crone

2020

Front. Syst. Neurosci.

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Respiratory motor failure is the leading cause of death in spinal cord injury (SCI). Cervical injuries disrupt connections between brainstem neurons that are the primary source of excitatory drive to respiratory motor neurons in the spinal cord and their targets. In addition to direct connections from bulbospinal neurons, respiratory motor neurons also receive excitatory and inhibitory inputs from propriospinal neurons, yet their role in the control of breathing is often overlooked. In this review, we will present evidence that propriospinal neurons play important roles in patterning muscle activity for breathing. These roles likely include shaping the pattern of respiratory motor output, processing and transmitting sensory afferent information, coordinating ventilation with motor activity, and regulating accessory and respiratory muscle activity. In addition, we discuss recent studies that have highlighted the importance of propriospinal neurons for recovery of respiratory muscle function following SCI. We propose that molecular genetic approaches to target specific developmental neuron classes in the spinal cord would help investigators resolve the many roles of propriospinal neurons in the control of breathing. A better understanding of how spinal circuits pattern breathing could lead to new treatments to improve breathing following injury or disease.

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A V0 core neuronal circuit for inspiration

Cited by 54 publications

References 67 publications

Phrenic motoneuron structural plasticity across models of diaphragm muscle paralysis

Phrenic motoneuron structural plasticity across models of diaphragm muscle paralysis

Dbx1 pre-Bötzinger complex interneurons comprise the core inspiratory oscillator for breathing in adult mice

Role of Propriospinal Neurons in Control of Respiratory Muscles and Recovery of Breathing Following Injury

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