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Hierarchy of orofacial rhythms revealed through whisking and breathing

Abstract

Whisking and sniffing are predominant aspects of exploratory behaviour in rodents. Yet the neural mechanisms that generate and coordinate these and other orofacial motor patterns remain largely uncharacterized. Here we use anatomical, behavioural, electrophysiological and pharmacological tools to show that whisking and sniffing are coordinated by respiratory centres in the ventral medulla. We delineate a distinct region in the ventral medulla that provides rhythmic input to the facial motor neurons that drive protraction of the vibrissae. Neuronal output from this region is reset at each inspiration by direct input from the pre-Bötzinger complex, such that high-frequency sniffing has a one-to-one relationship with whisking, whereas basal respiration is accompanied by intervening whisks that occur between breaths. We conjecture that the respiratory nuclei, which project to other premotor regions for oral and facial control, function as a master clock for behaviours that coordinate with breathing.

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Figure 1: Coordination of whisking and breathing.
Figure 2: Facial muscle activity during whisking and breathing.
Figure 3: Activity in medullary respiratory centres during breathing and whisking.
Figure 4: Injection of kainic acid in the medullary reticular formation induces whisking.
Figure 5: Lesion of the vIRt impairs ipsilateral whisking.
Figure 6: Anatomical evidence for connections between respiratory and whisking zones.
Figure 7: The whisking rhythm generator circuit in the broader context of orofacial behaviours.

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Acknowledgements

We thank A. Kepecs and F. Wang for sharing unpublished work, and these colleagues as well as M. S. Fee, J. L. Feldman, H. J. Karten, P. M. Knutsen, D. W. Matthews and K. Svoboda for discussions. We also thank K. Svoboda for sponsorship of the mouse experiments, M. Agrochao and B. el Jundi for assistance with these experiments, T. Ito and D. L. Oliver for use of their GlyT2 probe, K. K. Baldwin for the gift of the Sindbis viral vector and K. Yang for assistance with behavioural training. We are grateful to the Canadian Institutes of Health Research (grant MT-5877), the Howard Hughes Medical Institute, the Japan Society for the Promotion of Science (KAKENHI grants 23135519 and 24500409), the National Institutes of Health (grants NS058668, NS066664 and NS047101) and the US–Israeli Binational Science Foundation (grant 2003222).

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Authors

Contributions

M.D., D.K. and J.D.M. planned the experiments and wrote the manuscript. M.D., T.F. and J.D.M. carried out the rat experiments with assistance from M.D. for the histology and vibrissae tracking. D.H. carried out the mouse experiments with surgical assistance from M.C.S. Data analysis was carried out by J.D.M. with methodological contributions from D.K.

Corresponding authors

Correspondence to Martin Deschênes or David Kleinfeld.

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Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1-14 (PDF 9118 kb)

Kainic acid-induced whisking in a lightly anesthetized rat

Coordinated rhythmic movement of the ipsilateral vibrissae occurs after iontophoresis of kainic acid into the left ventral medulla. The same rat is shown both 60 and 160 minutes after the injection. All vibrissae except numbers C1 to C3 are clipped, and the video is displayed at 0.25-times the original speed. (WMV 2074 kb)

Whisking after electrolytic lesion of the vIRt in a freely moving rat

A lesion in the left vIRt impairs movement of the ipsilateral vibrissae. Quantification of the whisking behavior and the extent of the lesion in this rat is shown in Figure 5a-c. All vibrissae except numbers C1 to C4 are clipped, and the video is displayed at 0.30-times the original speed. (WMV 942 kb)

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Moore, J., Deschênes, M., Furuta, T. et al. Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature 497, 205–210 (2013). https://doi.org/10.1038/nature12076

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