Supra-orbital whiskers act as wind-sensing antennae in rats

Matias Mugnaini; Dhruv Mehrotra; Federico Davoine; Varun Sharma; Ana Rita Mendes; Ben Gerhardt; Miguel Concha-Miranda; Michael Brecht; Ann M Clemens

doi:10.1371/journal.pbio.3002168

Supra-orbital whiskers act as wind-sensing antennae in rats

PLoS Biol. 2023 Jul 6;21(7):e3002168. doi: 10.1371/journal.pbio.3002168. eCollection 2023 Jul.

Authors

Matias Mugnaini^{1

2}, Dhruv Mehrotra^{1

3

4}, Federico Davoine^{1

5}, Varun Sharma^{1

6}, Ana Rita Mendes^{1

7}, Ben Gerhardt⁸, Miguel Concha-Miranda⁸, Michael Brecht^{1

8}, Ann M Clemens^{1

9}

Affiliations

¹ Neural Systems & Behavior, Marine Biological Laboratory, Woods Hole, Massachusetts, United States of America.
² Laboratory of Physiology and Algorithms of the Brain, Leloir Institute (IIBBA-CONICET), Buenos Aires, Argentina.
³ Integrated Program in Neuroscience, McGill University, Montréal, Québec, Canada.
⁴ Montreal Neurological Institute and Hospital, Montréal, Québec, Canada.
⁵ Instituto de Ingeniería Eléctrica, Facultad de Ingeniería, Universidad de la República, Montevideo, Uruguay.
⁶ School of Biological Sciences & Graduate Program in Quantitative Biosciences, Georgia Institute of Technology, Atlanta, Georgia, United States of America.
⁷ Champalimaud Neuroscience Programme; Champalimaud Foundation, Doca de Pedrouços, Lisbon, Portugal.
⁸ Bernstein Center for Computational Neuroscience, Humboldt University of Berlin, Berlin, Germany.
⁹ University of Edinburgh, Simons Initiative for the Developing Brain, Edinburgh, Scotland, United Kingdom.

Abstract

We know little about mammalian anemotaxis or wind sensing. Recently, however, Hartmann and colleagues showed whisker-based anemotaxis in rats. To investigate how whiskers sense airflow, we first tracked whisker tips in anesthetized rats under low (0.5 m/s) and high (1.5 m/s) airflow. Whisker tips showed increasing movement from low to high airflow conditions, with all whisker tips moving during high airflow. Low airflow conditions-most similar to naturally occurring wind stimuli-engaged whisker tips differentially. Most whiskers moved little, but the long supra-orbital (lSO) whisker showed maximal displacement, followed by the α, β, and A1 whiskers. The lSO whisker differs from other whiskers in its exposed dorsal position, upward bending, length and thin diameter. Ex vivo extracted lSO whiskers also showed exceptional airflow displacement, suggesting whisker-intrinsic biomechanics mediate the unique airflow-sensitivity. Micro computed tomography (micro-CT) revealed that the ring-wulst-the follicle structure receiving the most sensitive afferents-was more complete/closed in the lSO, and other wind-sensitive whiskers, than in non-wind-sensitive whiskers, suggesting specialization of the supra-orbital for omni-directional sensing. We localized and targeted the cortical supra-orbital whisker representation in simultaneous Neuropixels recordings with D/E-row whisker barrels. Responses to wind-stimuli were stronger in the supra-orbital whisker representation than in D/E-row barrel cortex. We assessed the behavioral significance of whiskers in an airflow-sensing paradigm. We observed that rats spontaneously turn towards airflow stimuli in complete darkness. Selective trimming of wind-responsive whiskers diminished airflow turning responses more than trimming of non-wind-responsive whiskers. Lidocaine injections targeted to supra-orbital whisker follicles also diminished airflow turning responses compared to control injections. We conclude that supra-orbital whiskers act as wind antennae.

Copyright: © 2023 Mugnaini et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

MeSH terms

Animals
Mammals
Movement / physiology
Physical Stimulation
Rats
Somatosensory Cortex* / physiology
Vibrissae* / physiology
X-Ray Microtomography

Grants and funding

This work was supported by the Marine Biological Laboratory (MM, DM, FD, VS, ARM, MB, AC), a training grant from the NIMH (R25MH059472; MM, DM, FD, VS, ARM), Humboldt Universität zu Berlin, the Bernstein Center for Computational Neuroscience Berlin (MC, BG, MB), the German federal ministry of education and research (MB). AC is supported by the Simons Initiative for the Developing Brain, the University of Edinburgh and a Simons ESAT fellowship. ARM was supported by QuantOCancer and The Grass Foundation and DM was supported by The Grass Foundation to attend the Neural Systems & Behavior Course (NS&B). FD was supported by the Stanley W. Watson Education Fund to attend NS&B. MM was supported by an IBRO-USCRC Fellowship to attend NS&B. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.