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Supraorbital whiskers act as wind-antennae in rat anemotaxis

View ORCID ProfileMatias Mugnaini, View ORCID ProfileDhruv Mehrotra, View ORCID ProfileFederico Davoine, Varun Sharma, View ORCID ProfileAna Rita Mendes, Ben Gerhardt, View ORCID ProfileMiguel Concha-Miranda, View ORCID ProfileMichael Brecht, View ORCID ProfileAnn M. Clemens
doi: https://doi.org/10.1101/2022.08.18.504295
Matias Mugnaini
1Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543 USA
2Laboratory of Physiology and Algorithms of the Brain, Leloir Institute (IIBBA-CONICET), Av. Patricias Argentinas 435, Buenos Aires, Argentina
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Dhruv Mehrotra
1Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543 USA
3Integrated Program in Neuroscience, McGill University, 845 Sherbrooke St W, Montreal, QC, Canada
4Montreal Neurological Institute and Hospital, McGill University, Montreal, QC, Canada
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Federico Davoine
1Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543 USA
5Instituto de Ingeniería Eléctrica, Facultad de Ingeniería, Universidad de la República, 3RJM+898, Montevideo, Uruguay
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Varun Sharma
1Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543 USA
6School of Biological Sciences & Graduate Program in Quantitative Biosciences, Georgia Institute of Technology, North Ave NW, Atlanta, GA, 30332 USA
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Ana Rita Mendes
1Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543 USA
7Champalimaud Neuroscience Programme; Champalimaud Foundation, Av. Brasília, Doca de Pedrouços, 1400-038 Lisbon, Portugal
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Ben Gerhardt
8Bernstein Center for Computational Neuroscience, Humboldt University of Berlin, Philippstr. 13 Haus 6, 10115 Berlin, Germany
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Miguel Concha-Miranda
8Bernstein Center for Computational Neuroscience, Humboldt University of Berlin, Philippstr. 13 Haus 6, 10115 Berlin, Germany
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Michael Brecht
1Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543 USA
8Bernstein Center for Computational Neuroscience, Humboldt University of Berlin, Philippstr. 13 Haus 6, 10115 Berlin, Germany
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  • For correspondence: aclemens@ed.ac.uk
Ann M. Clemens
1Neural Systems & Behavior, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543 USA
9University of Edinburgh, Simons Initiative for the Developing Brain, 1 George Square, EH8 9JZ, Edinburgh, Scotland, United Kingdom
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  • For correspondence: aclemens@ed.ac.uk
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Abstract

We know little about mammalian anemotaxis, wind-sensing. Recently, however, Hartmann and colleagues showed whisker-based anemotaxis in rats. To investigate how whiskers sense airflow, we tracked whisker tips in anesthetized or cadaver rats under no airflow, low airflow and high (fan-blowing) airflow. Whisker tips showed little movement under no airflow conditions and all whisker tips moved during high airflow. Low airflow conditions – most similar to naturally occurring wind stimuli – engaged whisker tips differentially. Most whiskers moved little, the long supraorbital whisker showed maximal displacement and α, A1, β, and γ whiskers also showed movements. The long supraorbital whisker differs from other whiskers in its exposed dorsal position, upward bending, length and thin diameter. Ex vivo extracted long supraorbital whiskers also showed exceptional airflow displacement, suggesting whisker-intrinsic biomechanics mediate the unique airflow-sensitivity. Micro computed tomography revealed that the ring-wulst – the follicle structure receiving the most sensitive afferents – was more complete/ closed in supraorbital and other wind-sensitive whiskers than in non-wind-sensitive whiskers, suggesting specialization of the supraorbital for omni-directional sensing. We localized and targeted the cortical supraorbital whisker representation in simultaneous Neuropixels recordings with D/E-row whisker barrels. Responses to wind-stimuli were stronger in the supraorbital 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 supraorbital whisker follicles also diminished airflow turning responses compared to control injections. We conclude that supraorbital whiskers act as wind antennae.

New and Noteworthy Animals rely on sensory processing of airflow (anemotaxis) to guide navigation and survival. We examined mechanisms of rat anemotaxis by combining whisker tracking, biomechanical analysis, micro computed tomography of follicle structure, Neuropixels recordings in the barrel field, behavior of airflow turning and whisker interference by trimming and lidocaine injections. This diversity of methods led to a coherent pattern of results. Whiskers greatly differ in their airflow sensitivity and strongly wind-responsive whiskers – in particular long supraorbital whiskers – determine behavioral responses to airflow stimuli in rats.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵‡ shared senior authorship

  • We have added micro-CT imaging of the whisker follicle, revealing differential characteristics of the ring-wulst for supraorbital whiskers. We have additionally performed simultaneous Neuropixel recordings in the supraorbital and D/E row barrel map. We find that neuronal response of the supraorbital barrel region is sensitive to wind stimuli. Additional updates include more in-depth statistical analysis and minor text changes.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted December 02, 2022.
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Supraorbital whiskers act as wind-antennae in rat anemotaxis
Matias Mugnaini, Dhruv Mehrotra, Federico Davoine, Varun Sharma, Ana Rita Mendes, Ben Gerhardt, Miguel Concha-Miranda, Michael Brecht, Ann M. Clemens
bioRxiv 2022.08.18.504295; doi: https://doi.org/10.1101/2022.08.18.504295
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Supraorbital whiskers act as wind-antennae in rat anemotaxis
Matias Mugnaini, Dhruv Mehrotra, Federico Davoine, Varun Sharma, Ana Rita Mendes, Ben Gerhardt, Miguel Concha-Miranda, Michael Brecht, Ann M. Clemens
bioRxiv 2022.08.18.504295; doi: https://doi.org/10.1101/2022.08.18.504295

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