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Respiratory Rhythm Entrainment by Somatic Afferent Stimulation
Open accessAbstract
Respiratory and locomotor patterns are coupled during locomotion. The objectives of this study were to (1) demonstrate that respiratory rhythms are entrained by sensory input from somatic afferents, (2) establish whether the parabrachial nucleus mediates entrainment, (3) examine responses of single respiratory neurons in the ventral respiratory group (VRG) to somatic afferent stimulation, and (4) use a computational model of the pontomedullary respiratory network (Rybak et al., 2004a,b) to suggest neuronal mechanisms for entrainment. We used an in situ preparation in young rats that retained pontomedullary respiratory circuits and spinal pathways transmitting somatosensory input. We demonstrate that rhythmic stimulation of somatic afferents entrains respiratory rhythm on a 1:1 basis (1:1), increasing breathing frequency up to ∼1.4-2.2 times greater than spontaneous frequency. Stable entrainment occurred only when stimuli were delivered during expiration. Reversible blockade of the lateral parabrachial nucleus eliminated entrainment. Somatic afferent stimulation produced significant increases in the firing rate of augmenting expiratory (E2) neurons but shortened the firing duration of postinspiratory (post-I) neurons. A computational model reproduced 1:1 entrainment and other experimental findings based on the assumption that the somatic afferents initiate early onset of inspiration via activation of medullary E2 neurons. The model also predicted that afferent stimulation evoked transient hyperpolarization of ramp-inspiratory (ramp-I) neurons. This was confirmed experimentally by intracellular recording from ramp-I neurons. Our experimental and modeling results demonstrate that an entrainment pathway from somatic afferents to the VRG via the lateral parabrachial nucleus causes resetting of respiratory rhythm through excitation of E2 and consequent inhibition of post-I neurons.
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“Somatic afferent stimulation contributes to this entrainment, which can be prevented by blockade of the PB nucleus (cf Daley and Usherwood 2010; Porterfield 1985; Potts et al. 2005).”
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“Somatic afferent stimulation contributes to this entrainment, which can be prevented by blockade of the PB nucleus (cf Daley and Usherwood 2010; Porterfield 1985; Potts et al. 2005).”
BackgroundStructural and functional architecture of respiratory networks in the mammalian brainstem
Smith, J. C., Abdala, A. P., Rybak, I. A., & Paton, J. F. R. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0081 · Cited by 284
Self-citation
Metadata
- Authors
- Potts, J. T., Rybak, I. A., & Paton, J. F. R.
- Affiliations
- Wayne State University (US)
- Drexel University (US)
- University of Bristol (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-02-23
- Volume
- 25
- Issue
- 8
- Pages
- 1965-1978
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6726065
- OpenAlex
- W1983775575
- Cited by
- 128
- References
- 75
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 6 · 2022: 7 · 2021: 7 · 2020: 5 · 2019: 5 · 2018: 4 · 2017: 4 · 2016: 11 · 2015: 8 · 2014: 5 · 2013: 1 · 2012: 11
- FWCI
- 4.03
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Explore Bristol Research (publishedVersion)
- Funders
- British Heart Foundation
- Children's Hospital of Michigan
- National Institutes of Health
- National Heart, Lung, and Blood Institute (HL059167, R01HL072415, HL072415-01, R01HL059167)
- National Institute of Neurological Disorders and Stroke (NS046062-2, R01NS046062)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory and Cough-Related Research
- Keywords
- somatosensory input, parabrachial nucleus, ventral respiratory group, expiratory neurons
- MeSH terms
- Afferent Pathways, Animals, Inhalation, Computer Simulation, Decerebrate State, Forelimb, Isonicotinic Acids, Locomotion, Microinjections, Models, Neurological, Muscle Contraction, Neurons, Phrenic Nerve, Respiratory Center, Respiratory Physiological Phenomena, Time Factors, Vagus Nerve, Patch-Clamp Techniques, Rats, GABA-A Receptor Agonists, In Vitro Techniques
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