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

• Published in: PLoS biology Vol. 21; no. 7; p. e3002168
• Main Authors: Mugnaini, Matias, Mehrotra, Dhruv, Davoine, Federico, Sharma, Varun, Mendes, Ana Rita, Gerhardt, Ben, Concha-Miranda, Miguel, Brecht, Michael, Clemens, Ann M
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 06-07-2023; Public Library of Science (PLoS)
• Subjects: Air flow; Analysis; Anemotaxis; Antennae; Appendages (Animal anatomy); Barrels; Biology and Life Sciences; Biomechanics; Computed tomography; Cortex (barrel); Cortex (somatosensory); Darkness; Displacement; Earth Sciences; Follicles; Hyperstriatum; Insects; Lidocaine; Medicine and Health Sciences; Movement; Physical Sciences; Physiological aspects; Rats; Rattus; Representations; Research and Analysis Methods; Social Sciences; Stimuli; Tips; Trimming; Wind; Germany
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3002168

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.