The cellular basis of mechanosensation in mammalian tongue
Yalda Moayedi,
Shan Xu,
Sophie K. Obayashi,
Benjamin U. Hoffman,
Gregory J. Gerling,
Ellen A. Lumpkin
Affiliations
Yalda Moayedi
Department of Physiology and Cellular Biophysics, Columbia University, New York, NY 10032, USA; Department of Neurology, Columbia University, New York, NY 10032, USA; Department of Otolaryngology – Head & Neck Surgery, Columbia University, New York, NY 10032, USA
Shan Xu
School of Engineering and Applied Science, University of Virginia, Charlottesville, VA 22904, USA
Sophie K. Obayashi
Department of Molecular & Cell Biology, Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA
Benjamin U. Hoffman
Department of Physiology and Cellular Biophysics, Columbia University, New York, NY 10032, USA
Gregory J. Gerling
School of Engineering and Applied Science, University of Virginia, Charlottesville, VA 22904, USA; Corresponding author
Ellen A. Lumpkin
Department of Physiology and Cellular Biophysics, Columbia University, New York, NY 10032, USA; Department of Molecular & Cell Biology, Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA; Corresponding author
Summary: Mechanosensory neurons that innervate the tongue provide essential information to guide feeding, speech, and social grooming. We use in vivo calcium imaging of mouse trigeminal ganglion neurons to identify functional groups of mechanosensory neurons innervating the anterior tongue. These sensory neurons respond to thermal and mechanical stimulation. Analysis of neuronal activity patterns reveal that most mechanosensory trigeminal neurons are tuned to detect moving stimuli across the tongue. Using an unbiased, multilayer hierarchical clustering approach to classify pressure-evoked activity based on temporal response dynamics, we identify five functional classes of mechanosensory neurons with distinct force-response relations and adaptation profiles. These populations are tuned to detect different features of touch. Molecular markers of functionally distinct clusters are identified by analyzing cluster representation in genetically marked neuronal subsets. Collectively, these studies provide a platform for defining the contributions of functionally distinct mechanosensory neurons to oral behaviors crucial for survival in mammals.