Mechanisms of Efferent-Mediated Responses in the Turtle Posterior Crista

Holt, Joseph C.; Lysakowski, Anna; Goldberg, Jay M.

doi:10.1523/jneurosci.3539-06.2006

Cited by 54 publications

(102 citation statements)

References 66 publications

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“…As described in previous studies (Brichta and Goldberg 2000b;Holt et al 2006a), the B afferents recorded in this preparation are inhibited when shock trains are delivered to efferent fibers; the inhibition is associated with a reduction in quantal rate and represents an action on hair cells. In contrast, CD afferents are excited by efferent activation; the excitation is the result of a direct EPSP on the afferent and is not associated with a change in quantal rate.…”

Section: Resultssupporting

confidence: 63%

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Quantal and Nonquantal Transmission in Calyx-Bearing Fibers of the Turtle Posterior Crista

Holt

Chatlani

Lysakowski³

et al. 2007

Journal of Neurophysiology

107

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Intracellular recordings were made from nerve fibers in the posterior ampullary nerve near the neuroepithelium. Calyx-bearing afferents were identified by their distinctive efferent-mediated responses. Such fibers receive inputs from both type I and type II hair cells. Type II inputs are made by synapses on the outer face of the calyx ending and on the boutons of dimorphic fibers. Quantal activity, consisting of brief mEPSPs, is reduced by lowering the external concentration of Ca 2+ and blocked by the AMPA-receptor antagonist CNQX. Poisson statistics govern the timing of mEPSPs, which occur at high rates (250-2,500/s) in the absence of mechanical stimulation. Excitation produced by canal-duct indentation can increase mEPSP rates to nearly 5,000/s. As the rate increases, mEPSPs can change from a monophasic depolarization to a biphasic depolarizinghyperpolarizing sequence, both of whose components are blocked by CNQX. Blockers of voltagegated currents affect mEPSP size, which is decreased by TTX and is increased by linopirdine. mEPSP size decreases several fold after impalement. The size decrease, although it may be triggered by the depolarization occurring during impalement, persists even at hyperpolarized membrane potentials. Nonquantal transmission is indicated by shot-noise calculations and by the presence of voltage modulations after quantal activity is abolished pharmacologically. An ultrastructural study shows that inner-face inputs from type I hair cells outnumber outer-face inputs from type II hair cells by an almost 6:1 ratio.

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Section: Resultssupporting

confidence: 63%

“…Inspection of individual records indicated that there was no obvious change in quantal variance during the EPSP (Fig. 2B), which was confirmed with ensemble averages (see Holt et al 2006a). In the first minute after impalement, the unit had a resting membrane potential of −47 mV (Fig.…”

Section: Synaptic Transmission In CD Unitssupporting

confidence: 67%

Quantal and Nonquantal Transmission in Calyx-Bearing Fibers of the Turtle Posterior Crista

Holt

Chatlani

Lysakowski³

et al. 2007

Journal of Neurophysiology

107

View full text Add to dashboard Cite

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“…As described previously (Holt et al 2006a(Holt et al , 2006b(Holt et al , 2007, red-eared slider turtles (Trachemys scripta elegans) of either sex were decapitated and the head was split parasagitally. A half head was mounted in a recording chamber kept at room temperature (21-23°C), viewed with a dissecting microscope, and continually superfused with an oxygenated solution containing (in mM) 105 NaCl, 4 KCl, 0.8 MgCl 2 , 2 CaCl 2 , 25 NaHCO 3 , 2 sodium pyruvate, and 10 glucose, at a pH of 7.2-7.3 after bubbling with 95% O 2 -5% CO 2 .…”

Section: Preparationmentioning

confidence: 99%

“…Efferent fibers located in a connecting branch between the superior and inferior vestibular nerves were electrically stimulated (Brichta and Goldberg 2000b;Holt et al 2006a). Afferents could be distinguished by their efferent responses.…”

Section: Preparationmentioning

confidence: 99%

Discharge regularity in the turtle posterior crista: comparisons between experiment and theory

Goldberg

Holt

2013

Journal of Neurophysiology

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Goldberg JM, Holt JC. Discharge regularity in the turtle posterior crista: comparisons between experiment and theory. J Neurophysiol 110: 2830 -2848, 2013. First published September 4, 2013 doi:10.1152/jn.00195.2013.-Intra-axonal recordings were made from bouton fibers near their termination in the turtle posterior crista. Spike discharge, miniature excitatory postsynaptic potentials (mEPSPs), and afterhyperpolarizations (AHPs) were monitored during resting activity in both regularly and irregularly discharging units. Quantal size (qsize) and quantal rate (qrate) were estimated by shot-noise theory. Theoretically, the ratio, V /(d V /dt), between synaptic noise ( V ) and the slope of the mean voltage trajectory (d V /dt) near threshold crossing should determine discharge regularity. AHPs are deeper and more prolonged in regular units; as a result, d V /dt is larger, the more regular the discharge. The qsize is larger and qrate smaller in irregular units; these oppositely directed trends lead to little variation in V with discharge regularity. Of the two variables, d V /dt is much more influential than the nearly constant V in determining regularity. Sinusoidal canal-duct indentations at 0.3 Hz led to modulations in spike discharge and synaptic voltage. Gain, the ratio between the amplitudes of the two modulations, and phase leads re indentation of both modulations are larger in irregular units. Gain variations parallel the sensitivity of the postsynaptic spike encoder, the set of conductances that converts synaptic input into spike discharge. Phase variations reflect both synaptic inputs to the encoder and postsynaptic processes. Experimental data were interpreted using a stochastic integrate-and-fire model. Advantages of an irregular discharge include an enhanced encoder gain and the prevention of nonlinear phase locking. Regular and irregular units are more efficient, respectively, in the encoding of low-and high-frequency head rotations, respectively. discharge regularity; miniature excitatory postsynaptic potentials; afterhyperpolarizations; integrate-and-fire model; coding efficiency

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“…The extent to which this active process is physiologically relevant to semicircular canal vestibular sensation is unclear. Analogous to the mammalian cochlea and other auditory organs, the vestibular semicircular canals generally receive an extensive efferent innervation that controls sensitivity to physiological stimuli (27)(28)(29)(30), but it is not known if efferent activation alters hair-bundle motion or amplification. These and related data compel the hypothesis that vestibular organs are active electromechanical amplifiers that are controlled by the brain via the efferent system.…”

mentioning

confidence: 99%

Mechanical amplification by hair cells in the semicircular canals

Rabbitt

Boyle

Highstein

2010

Proc. Natl. Acad. Sci. U.S.A.

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Sensory hair cells are the essential mechanotransducers of the inner ear, responsible not only for the transduction of sound and motion stimuli but also, remarkably, for nanomechanical amplification of sensory stimuli. Here we show that semicircular canal hair cells generate a mechanical nonlinearity in vivo that increases sensitivity to angular motion by amplification at low stimulus strengths. Sensitivity at high stimulus strengths is linear and shows no evidence of amplification. Results suggest that the mechanical work done by hair cells contributes ∼97 zJ/cell of amplification per stimulus cycle, improving sensitivity to angular velocity stimuli below ∼5°/s (0.3-Hz sinusoidal motion). We further show that mechanical amplification can be inhibited by the brain via activation of efferent synaptic contacts on hair cells. The experimental model was the oyster toadfish, Opsanus tau. Physiological manifestation of mechanical amplification and efferent control in a teleost vestibular organ suggests the active motor process in sensory hair cells is ancestral. The biophysical basis of the motor(s) remains hypothetical, but a key discriminating question may involve how changes in somatic electrical impedance evoked by efferent synaptic action alter function of the motor(s).active process | auditory | hair bundle | inner ear | motor V estibular organs resembling those of modern humans first appeared in primitive fish over 400 million years ago (1) and have remained relatively unchanged to provide sensations of gravity, motion, and vibration. These inner-ear organs rely on sensory hair cells to convert mechanical motion of their microvilli (stereocilia) bundle at the apical end of the cell into synaptic neural transmission at the basal end. In auditory organs, hair cells are known to have a dual role and serve not only as mechanosensitive transducers but also as motors that mechanically amplify quiet sounds within the ear (2). In mammals this amplification is partially the result of piezoelectric-like somatic electromotility of cochlear outer hair cells (3), motility that requires expression of the protein prestin in the plasma membrane (4, 5). Hair-cell amplification is controlled by the brain through an extensive centripetal efferent innervation in the cochlea synapsing on outer hair cells (6). Activation of medial olivocochlear efferent neurons sharply reduces the mechanical vibration and tuning of the cochlear organ of Corti (7, 8) through the inhibitory action of efferent neurotransmitter(s) on the motor output of outer hair cells (9, 10). Taken together, these findings reveal that the mammalian cochlea is an active electromechanical amplifier controlled by the brain to be exquisitely sensitive to low sound pressure levels of interest to the organism. Whether an amplification strategy is a general principle of sensory hair-cell organs or is limited to a subset of hearing organs remains a topic of debate. We know that somatic electromotility and the protein prestin are specialized to the mammalian cochlea and are n...

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Mechanisms of Efferent-Mediated Responses in the Turtle Posterior Crista

Cited by 54 publications

References 66 publications

Quantal and Nonquantal Transmission in Calyx-Bearing Fibers of the Turtle Posterior Crista

Quantal and Nonquantal Transmission in Calyx-Bearing Fibers of the Turtle Posterior Crista

Discharge regularity in the turtle posterior crista: comparisons between experiment and theory

Mechanical amplification by hair cells in the semicircular canals

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