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Research Articles, Systems/Circuits

Descending Modulation of Laryngeal Vagal Sensory Processing in the Brainstem Orchestrated by the Submedius Thalamic Nucleus

Stuart B. Mazzone, Tara G. Bautista, Anthony J. M. Verberne, Matthew W. Trewella, Michael J. Farrell and Alice E. McGovern
Journal of Neuroscience 2 December 2020, 40 (49) 9426-9439; DOI: https://doi.org/10.1523/JNEUROSCI.2430-20.2020
Stuart B. Mazzone
1Department of Anatomy and Neuroscience, The University of Melbourne, Parkville 3010, Victoria, Australia
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Tara G. Bautista
1Department of Anatomy and Neuroscience, The University of Melbourne, Parkville 3010, Victoria, Australia
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Anthony J. M. Verberne
2Clinical Pharmacology and Therapeutics Unit, Department of Medicine, Austin Health, The University of Melbourne, Heidelberg 3084, Victoria, Australia
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Matthew W. Trewella
1Department of Anatomy and Neuroscience, The University of Melbourne, Parkville 3010, Victoria, Australia
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Michael J. Farrell
3Department of Medical Imaging and Radiation Sciences and Monash Biomedical Imaging, Monash University, Clayton 3800, Victoria, Australia
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Alice E. McGovern
1Department of Anatomy and Neuroscience, The University of Melbourne, Parkville 3010, Victoria, Australia
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Abstract

The nodose and jugular vagal ganglia supply sensory innervation to the airways and lungs. Jugular vagal airway sensory neurons wire into a brainstem circuit with ascending projections into the submedius thalamic nucleus (SubM) and ventrolateral orbital cortex (VLO), regions known to regulate the endogenous analgesia system. Here we investigate whether the SubM–VLO circuit exerts descending regulation over airway vagal reflexes in male and female rats using a range of neuroanatomical tracing, reflex physiology, and chemogenetic techniques. Anterograde and retrograde neuroanatomical tracing confirmed the connectivity of the SubM and VLO. Laryngeal stimulation in anesthetized rats reduced respiration, a reflex that was potently inhibited by activation of SubM. Conversely, inhibition of SubM potentiated laryngeal reflex responses, while prior lesions of VLO abolished the effects of SubM stimulation. In conscious rats, selective chemogenetic activation of SubM neurons specifically projecting to VLO significantly inhibited respiratory responses evoked by inhalation of the nociceptor stimulant capsaicin. Jugular vagal inputs to SubM via the medullary paratrigeminal nucleus were confirmed using anterograde transsynaptic conditional herpes viral tracing. Respiratory responses evoked by microinjections of capsaicin into the paratrigeminal nucleus were significantly attenuated by SubM stimulation, whereas those evoked via the nucleus of the solitary tract were unaltered. These data suggest that jugular vagal sensory pathways input to a nociceptive thalamocortical circuit capable of regulating jugular sensory processing in the medulla. This circuit organization suggests an intersection between vagal sensory pathways and the endogenous analgesia system, potentially important for understanding vagal sensory processing in health and mechanisms of hypersensitivity in disease.

SIGNIFICANCE STATEMENT Jugular vagal sensory pathways are increasingly recognized for their important role in defensive respiratory responses evoked from the airways. Jugular ganglia neurons wire into a central circuit that is notable for overlapping with somatosensory processing networks in the brain rather than the viscerosensory circuits in receipt of inputs from the nodose vagal ganglia. Here we demonstrate a novel and functionally relevant example of intersection between vagal and somatosensory processing in the brain. The findings of the study offer new insights into interactions between vagal and spinal sensory processing, including the medullary targets of the endogenous analgesia system, and offer new insights into the central processes involved in airway defense in health and disease.

  • airway innervation
  • jugular vagal ganglia
  • respiratory
  • submedius thalamic nucleus
  • vagus nerve
  • ventrolateral orbital cortex

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The Journal of Neuroscience: 40 (49)
Journal of Neuroscience
Vol. 40, Issue 49
2 Dec 2020
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Descending Modulation of Laryngeal Vagal Sensory Processing in the Brainstem Orchestrated by the Submedius Thalamic Nucleus
Stuart B. Mazzone, Tara G. Bautista, Anthony J. M. Verberne, Matthew W. Trewella, Michael J. Farrell, Alice E. McGovern
Journal of Neuroscience 2 December 2020, 40 (49) 9426-9439; DOI: 10.1523/JNEUROSCI.2430-20.2020

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Descending Modulation of Laryngeal Vagal Sensory Processing in the Brainstem Orchestrated by the Submedius Thalamic Nucleus
Stuart B. Mazzone, Tara G. Bautista, Anthony J. M. Verberne, Matthew W. Trewella, Michael J. Farrell, Alice E. McGovern
Journal of Neuroscience 2 December 2020, 40 (49) 9426-9439; DOI: 10.1523/JNEUROSCI.2430-20.2020
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Keywords

  • airway innervation
  • jugular vagal ganglia
  • respiratory
  • submedius thalamic nucleus
  • vagus nerve
  • ventrolateral orbital cortex

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