Somatosensory Substrates of Flight Control in Bats
Kara L. Marshall1, Mohit Chadha2, 3, Laura A. deSouza4, Susanne J. Sterbing-D’Angelo5, 6, Cynthia F. Moss2, 3, 5, 6, , , Ellen A. Lumpkin1, 4, ,
1 Departments of Dermatology and Physiology and Cellular Biophysics, Columbia University, New York, NY 10032, USA
2 Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD 20742, USA
3 Department of Psychology, University of Maryland, College Park, MD 20742, USA
4 Program in Neurobiology and Behavior, Columbia University, New York, NY 10032, USA
5 Institute for Systems Research, University of Maryland, College Park, MD 20742, USA
Received 8 December 2014, Revised 11 March 2015, Accepted 29 March 2015,
Available online 30 April 2015
Published: April 30, 2015
Highlights
• Segmental organization of wing innervation differs from known vertebrate forelimbs
• The bat wing has an atypical dermatome map that can be explained by its ontogeny
• Bat wings are equipped with an unusual repertoire of somatosensory receptors
• Sparse cortical coding represents inputs from biological airflow and touch sensors
Summary
Flight maneuvers require rapid sensory integration to generate adaptive motor output. Bats achieve remarkable agility with modified forelimbs that serve as airfoils while retaining capacity for object manipulation. Wing sensory inputs provide behaviorally relevant information to guide flight; however, components of wing sensory-motor circuits have not been analyzed. Here, we elucidate the organization of wing innervation in an insectivore, the big brown bat, Eptesicus fuscus. We demonstrate that wing sensory innervation differs from other vertebrate forelimbs, revealing a peripheral basis for the atypical topographic organization reported for bat somatosensory nuclei. Furthermore, the wing is innervated by an unusual complement of sensory neurons poised to report airflow and touch. Finally, we report that cortical neurons encode tactile and airflow inputs with sparse activity patterns. Together, our findings identify neural substrates of somatosensation in the bat wing and imply that evolutionary pressures giving rise to mammalian flight led to unusual sensorimotor projections.
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