Large basolateral processes on type II hair cells are novel processing units in mammalian vestibular organs

• Published in: Journal of comparative neurology (1911) Vol. 522; no. 14; pp. 3141 - 3159
• Main Authors: Pujol, Rémy, Pickett, Sarah B., Nguyen, Tot Bui, Stone, Jennifer S.
• Format: Journal Article
• Language: English
• Published: United States Blackwell Publishing Ltd 01.10.2014; Wiley Subscription Services, Inc
• Subjects: 000654; 000664; 737903; AB_10013626; AB_10015251; AB_10175616; AB_177520; AB_2068336; AB_2068506; AB_2079751; AB_2113875; AB_2282417; AB_2286684; AB_399431; AB_477329; Animals; Auditory Pathways - cytology; Auditory Pathways - metabolism; Calcium-Binding Proteins - metabolism; Cell Count; Chiroptera; Choline O-Acetyltransferase - metabolism; DNA-Binding Proteins - metabolism; Hair Cells, Vestibular - classification; Hair Cells, Vestibular - metabolism; Hair Cells, Vestibular - ultrastructure; JAX; mammal; Mammals - anatomy & histology; Mice; Microscopy, Electron, Transmission; morphology; Nerve Fibers - metabolism; Nerve Fibers - ultrastructure; Nerve Net - metabolism; Nerve Net - ultrastructure; Nerve Tissue Proteins - metabolism; Phosphoproteins - metabolism; Rats; RGD; SOXB1 Transcription Factors - metabolism; Species Specificity; synapse; type II hair cell; vestibular; Vestibule, Labyrinth - cytology; JAX; 737903; AB_2286684; morphology; 000654; 000664; AB_10015251; synapse; vestibular; AB_10175616; AB_2079751; AB_2113875; RGD; AB_2068506; AB_2282417; AB_2068336; mammal; AB_10013626; type II hair cell; AB_177520; AB_477329; AB_399431
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.23625

ABSTRACT Sensory receptors in the vestibular system (hair cells) encode head movements and drive central motor reflexes that control gaze, body movements, and body orientation. In mammals, type I and II vestibular hair cells are defined by their shape, contacts with vestibular afferent nerves, and membrane conductance. Here we describe unique morphological features of type II vestibular hair cells in mature rodents (mice and gerbils) and bats. These features are cytoplasmic processes that extend laterally from the hair cell base and project under type I hair cells. Closer analysis of adult mouse utricles demonstrated that the basolateral processes of type II hair cells vary in shape, size, and branching, with the longest processes extending three to four hair cell widths. The hair cell basolateral processes synapse upon vestibular afferent nerves and receive inputs from vestibular efferent nerves. Furthermore, some basolateral processes make physical contacts with the processes of other type II hair cells, forming some sort of network among type II hair cells. Basolateral processes are rare in perinatal mice and do not attain their mature form until 3–6 weeks of age. These observations demonstrate that basolateral processes are significant signaling regions of type II vestibular hair cells and suggest that type II hair cells may directly communicate with each other, which has not been described in vertebrates. J. Comp. Neurol. 522:3141–3159, 2014. © 2014 Wiley Periodicals, Inc. By using confocal and transmission electron microscopy, we identified novel morphological features of type II vestibular hair cells in mature mammals (mice, gerbils, and bats). These features are large basolateral extensions of cytoplasm that extend several cell lengths below the cell bodies of type I hair cells. These basolateral processes allow physical contacts between one or more type II hair cell and are rich sites for synapses between hair cells and afferent nerve fibers. Contact between mature mammalian vestibular hair cells is novel and suggests that some form of hair cell‐to‐hair cell communication occurs in vestibular organs.