Convergence of excitatory and inhibitory hair cell transmitters shapes vestibular afferent responses.

The vestibular semicircular canals respond to angular acceleration that is integrated to angular velocity by the biofluid mechanics of the canals and is the primary origin of afferent responses encoding velocity. Surprisingly, some afferents actually report angular acceleration. Our data indicate that hair-cell/afferent synapses introduce a mathematical derivative in these afferents that partially cancels the biomechanical integration and results in discharge rates encoding angular acceleration. We examined the role of convergent synaptic inputs from hair cells to this mathematical differentiation. A significant reduction in the order of the differentiation was observed for low-frequency stimuli after gamma-aminobutyric acid type B receptor antagonist administration. Results demonstrate that gamma-aminobutyric acid participates in shaping the temporal dynamics of afferent responses.

[1]  J. Goldberg,et al.  Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. , 1971, Journal of neurophysiology.

[2]  C. Yamamoto,et al.  Quantal analysis of suppressing action of baclofen on mossy fiber synapses in guinea pig hippocampus , 1992, Brain Research.

[3]  J. Ashmore,et al.  GABAB-mediated modulation of ionic conductances in type I hair cells isolated from guinea-pig semicircular canals , 1993, Brain Research.

[4]  B. Hille,et al.  Ionic channels of excitable membranes , 2001 .

[5]  R. Fitzpatrick,et al.  The vestibular system , 2005, Current Biology.

[6]  John H. Anderson,et al.  Neurochemistry of the Vestibular System , 2023 .

[7]  W. Steinhausen Über die Beobachtung der Cupula in den Bogengangsampullen des Labyrinths des lebenden Hechts , 1933, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[8]  R. Rabbitt,et al.  Determinants of Semicircular Canal Afferent Response Dynamics in Fish a , 1996, Annals of the New York Academy of Sciences.

[9]  J. Goldberg,et al.  Hair-cell counts and afferent innervation patterns in the cristae ampullares of the squirrel monkey with a comparison to the chinchilla. , 1995, Journal of neurophysiology.

[10]  David W Tank,et al.  Behavioral/systems/cognitive Correlated Discharge among Cell Pairs within the Oculomotor Horizontal Velocity-to-position Integrator Materials and Methods , 2022 .

[11]  R. Rabbitt,et al.  Mechanical indentation of the vestibular labyrinth and its relationship to head rotation in the toadfish, Opsanus tau. , 1995, Journal of neurophysiology.

[12]  S. Highstein,et al.  Morphological correlates of response dynamics and efferent stimulation in horizontal semicircular canal afferents of the toadfish, Opsanus tau. , 1991, Journal of neurophysiology.

[13]  O. Ottersen,et al.  Molecular organization of a type of peripheral glutamate synapse: the afferent synapses of hair cells in the inner ear , 1998, Progress in Neurobiology.

[14]  J. Goldberg,et al.  Structure and Function of Vestibular Nerve Fibers in the Chinchilla and Squirrel Monkey a , 1992, Annals of the New York Academy of Sciences.

[15]  M. Correia,et al.  Responses of pigeon horizontal semicircular canal afferent fibers. I. Step, trapezoid, and low-frequency sinusoid mechanical and rotational stimulation. , 1989, Journal of neurophysiology.

[16]  R. Rabbitt,et al.  Influence of surgical plugging on horizontal semicircular canal mechanics and afferent response dynamics. , 1999, Journal of neurophysiology.

[17]  M. Correia,et al.  A method for controlled mechanical stimulation of single semicircular canals , 1988, Journal of Neuroscience Methods.

[18]  J. Goldberg,et al.  The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. , 1988, Journal of neurophysiology.

[19]  R. Boyle,et al.  Resting discharge and response dynamics of horizontal semicircular canal afferents of the toadfish, Opsanus tau , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  I. Podlubny Fractional differential equations , 1998 .

[21]  R. Rabbitt,et al.  γ‐Aminobutyric acid is present in a spatially discrete subpopulation of hair cells in the crista ampullaris of the toadfish Opsanus tau , 2004, The Journal of comparative neurology.

[22]  L. Trussell,et al.  Enhancement of Synaptic Efficacy by Presynaptic GABAB Receptors , 1998, Neuron.

[23]  A. Lysakowski Synaptic Organization of the Crista Ampullaris in Vertebrates a , 1996, Annals of the New York Academy of Sciences.

[24]  M. Raiteri,et al.  International Union of Pharmacology. XXXIII. Mammalian γ-Aminobutyric AcidB Receptors: Structure and Function , 2002, Pharmacological Reviews.

[25]  P. Perin,et al.  The vestibular hair cells:post-transductional signal processing , 1998, Progress in Neurobiology.

[26]  P. Gage,et al.  GABAB agonists modulate a transient potassium current in cultured mammalian hippocampal neurons , 1990, Neuroscience Letters.

[27]  J. Goldberg,et al.  The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in the horizontal and superior semicircular canals. , 1988, Journal of neurophysiology.