The Journal of Neuroscience, December 20, 2006, 26(51):13180-13193; doi:10.1523/JNEUROSCI.3539-06.2006
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Cellular/Molecular
Mechanisms of Efferent-Mediated Responses in the Turtle Posterior Crista
Joseph C. Holt,1
Anna Lysakowski,2 and
Jay M. Goldberg1
1Department of Neurobiology, Pharmacology, and Physiology, University of Chicago, Chicago, Illinois 60637, and 2Department of Anatomy and Cell Biology, University of Illinois at Chicago, Chicago, Illinois 60612
Correspondence should be addressed to Joseph C. Holt at his present address: Department of Otolaryngology, University of Texas Medical Branch, 7.102 Medical Research Building, 301 University Boulevard, Galveston, TX 77555-1063. Email: jcholt{at}utmb.edu
To study the cellular mechanisms of efferent actions, we recorded from vestibular-nerve afferents close to the turtle posterior crista while efferent fibers were electrically stimulated. Efferent-mediated responses were obtained from calyx-bearing (CD, calyx and dimorphic) afferents and from bouton (B) afferents distinguished by their neuroepithelial locations into BT units near the torus and BM units at intermediate sites. The spike discharge of CD units is strongly excited by efferent stimulation, whereas BT and BM units are inhibited, with BM units also showing a postinhibitory excitation. Synaptic activity was recorded intracellularly after spikes were blocked. Responses of BT/BM units to single efferent shocks consist of a brief depolarization followed by a prolonged hyperpolarization. Both components reflect variations in hair-cell quantal release rates and are eliminated by pharmacological antagonists of
9/
10 nicotinic receptors. Blocking calcium-dependent SK potassium channels converts the biphasic response into a prolonged depolarization. Results can be explained, as in other hair-cell systems, by the sequential activation of
9/
10 and SK channels. In BM units, the postinhibitory excitation is based on an increased rate of hair-cell quanta and depends on the preceding inhibition. There is, in addition, an efferent-mediated, direct depolarization of BT/BM and CD fibers. In CD units, it is the exclusive efferent response. Nicotinic antagonists have different effects on hair-cell efferent actions and on the direct depolarization of CD and BT/BM units. Ultrastructural studies, besides confirming the efferent innervation of type II hair cells and calyx endings, show that turtle efferents commonly contact afferent boutons terminating on type II hair cells.
Key words: vestibular afferent; vestibular efferent; hair cell; nicotinic;
9; pharmacology
Received April 11, 2006;
revised Oct. 12, 2006;
accepted Nov. 6, 2006.
Correspondence should be addressed to Joseph C. Holt at his present address: Department of Otolaryngology, University of Texas Medical Branch, 7.102 Medical Research Building, 301 University Boulevard, Galveston, TX 77555-1063. Email: jcholt{at}utmb.edu
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