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Evidence for multiple sensory circuits in the brain arising from the respiratory system: an anterograde viral tract tracing study in rodents

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Abstract

Complex sensations accompany the activation of sensory neurons within the respiratory system, yet little is known about the organization of sensory pathways in the brain that mediate these sensations. In the present study, we employ anterograde viral neuroanatomical tract tracing with isogenic self-reporting recombinants of HSV-1 strain H129 to map the higher brain regions in receipt of vagal sensory neurons arising from the trachea versus the lungs, and single-cell PCR to characterize the phenotype of sensory neurons arising from these two divisions of the respiratory tree. The results suggest that the upper and lower airways are predominantly innervated by sensory neurons derived from the somatic jugular and visceral nodose cranial ganglia, respectively. This coincides with central circuitry that is predominately somatic-like, arising from the trachea, and visceral-like, arising from the lungs. Although some convergence of sensory pathways was noted in preautonomic cell groups, this was notably absent in thalamic and cortical regions. These data support the notion that distinct afferent subtypes, via distinct central circuits, subserve sensations arising from the upper versus lower airways. The findings may explain why sensations arising from different levels of the respiratory tree are qualitatively and quantitatively unique.

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Acknowledgments

This research was supported by grants to Dr Mazzone and Dr Farrell from the National Health and Medical Research Council (NHMRC) of Australia [566734, 454776, 1025589]. The authors would like to thank Professor Lynn Enquist and Dr Halina Staniszewska Goraczniak (Princeton University, Princeton, NJ, USA) for their generosity in supplying the original wild-type H129 strain of HSV-1 and to Professor Stacey Efstathiou (University of Cambridge, UK) for supplying the tdTomato expression cassette.

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Authors and Affiliations

  1. School of Biomedical Sciences, The University of Queensland, St Lucia, QLD, 4072, Australia

    Alice E. McGovern, Seung-Kwon Yang, David G. Simmons & Stuart B. Mazzone

  2. Clinical Medical Virology Centre/Queensland Children’s Medical Research Centre, The University of Queensland and Sir Albert Sakzewski Virus Research Centre, Royal Children’s Hospital, Brisbane, QLD, 4029, Australia

    Nicholas Davis-Poynter

  3. Department of Medical Imaging and Radiation Sciences, Monash University, Clayton, VIC, 3800, Australia

    Michael J. Farrell

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  1. Alice E. McGovern
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  2. Nicholas Davis-Poynter
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  3. Seung-Kwon Yang
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  4. David G. Simmons
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  5. Michael J. Farrell
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  6. Stuart B. Mazzone
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Correspondence to Alice E. McGovern.

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McGovern, A.E., Davis-Poynter, N., Yang, SK. et al. Evidence for multiple sensory circuits in the brain arising from the respiratory system: an anterograde viral tract tracing study in rodents. Brain Struct Funct 220, 3683–3699 (2015). https://doi.org/10.1007/s00429-014-0883-9

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  • DOI: https://doi.org/10.1007/s00429-014-0883-9

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