Ion channels in mammalian vestibular afferents may set regularity of firing

Eatock, Ruth Anne; Xue, Jianping; Kalluri, Radha

doi:10.1242/jeb.017350

Cited by 63 publications

(53 citation statements)

References 85 publications

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“…Vestibular afferent fibers display a wide range of firing patterns and are spontaneously active (Eatock et al, 2008). Spontaneous afferent activity is likely the result of release of transmitter from hair cells, since vestibular neurons in denervated preparations without hair cell end organs lack spontaneous activity (Risner and Holt, 2006; Kalluri et al, 2010; Trapani and Nicholson, 2011).…”

Section: Discussionmentioning

confidence: 99%

HCN Channels Expressed in the Inner Ear Are Necessary for Normal Balance Function

Horwitz¹,

Risner-Janiczek²,

Jones

et al. 2011

J. Neurosci.

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HCN1-4 subunits form Na+/K+ permeable ion channels that are activated by hyperpolarization and carry the current known as Ih. Ih has been characterized in vestibular hair cells of the inner ear, but its molecular correlates and functional contributions have not been elucidated. We examined Hcn mRNA expression and immunolocalization of HCN protein in the mouse utricle, a mechanosensitive organ that contributes to the sense of balance. We found that HCN1 is the most highly expressed subunit, localized to the basolateral membranes of type I and type II hair cells. We characterized Ih using the whole-cell, voltage-clamp technique and found the current expressed in ~90% of the cells with a mean maximum conductance of 4.4 nS. Ih was inhibited by ZD7288, Cilobradine and by adenoviral expression of a dominant-negative form of HCN2. To determine which HCN subunits carried Ih we examined hair cells from mice deficient in Hcn1, 2, or both. Ih was completely abolished in hair cells of Hcn1−/− mice and Hcn1,2−/− mice but was similar to wild-type in Hcn2−/− mice. To examine the functional contributions of Ih, we recorded hair cell membrane responses to small hyperpolarizing current steps and found that activation of Ih evoked a 5-10 mV sag depolarization and a subsequent 15-20 mV rebound upon termination. The sag and rebound were nearly abolished in Hcn1-deficient hair cells. We also found that Hcn1-deficient mice had deficits in vestibular evoked potentials and balance assays. We conclude that HCN1 contributes to vestibular hair cell function and the sense of balance.

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Section: Discussionmentioning

confidence: 99%

HCN Channels Expressed in the Inner Ear Are Necessary for Normal Balance Function

Horwitz¹,

Risner-Janiczek²,

Jones

et al. 2011

J. Neurosci.

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“…Compatible with the necessity for a functional organization of VOR circuitry into separate, frequency-tuned pathways [Straka et al, 2009], vestibular afferent fibers differ in several interrelated morphophysiological properties [Straka and Dieringer, 2004]. Independent of the classification scheme, these neurons form at least two functionally distinct subtypes with different cellular properties, dynamic capabilities and motion-related discharge profiles [Goldberg, 2000;Eatock et al, 2008;Cullen, 2011]. The decomposition and transformation of body motion by semicircular canal and otolith hair cells into electrical signals with different dynamic signatures is maintained at the level of the afferent fibers by connecting hair cells and afferents with matching response properties, illustrating a major functional principle of vestibular signal processing [Straka and Dieringer, 2004;Straka et al, 2009].…”

Section: Evolving An Ear and Connecting It To The Hindbrainmentioning

confidence: 99%

Connecting Ears to Eye Muscles: Evolution of a ‘Simple' Reflex Arc

2014

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Developmental and evolutionary data from vertebrates are beginning to elucidate the origin of the sensorimotor pathway that links gravity and motion detection to image-stabilizing eye movements - the vestibulo-ocular reflex (VOR). Conserved transcription factors coordinate the development of the vertebrate ear into three functional sensory compartments (graviception/translational linear acceleration, angular acceleration and sound perception). These sensory components connect to specific populations of vestibular and auditory projection neurons in the dorsal hindbrain through undetermined molecular mechanisms. In contrast, a molecular basis for the patterning of the vestibular projection neurons is beginning to emerge. These are organized through the actions of rostrocaudally and dorsoventrally restricted transcription factors into a ‘hodological mosaic' within which coherent and largely segregated subgroups are specified to project to different targets in the spinal cord and brain stem. A specific set of these regionally diverse vestibular projection neurons functions as the central element that transforms vestibular sensory signals generated by active and passive head and body movements into motor output through the extraocular muscles. The large dynamic range of motion-related sensory signals requires an organization of VOR pathways as parallel, frequency-tuned, hierarchical connections from the sensory periphery to the motor output. We suggest that eyes, ears and functional connections subserving the VOR are vertebrate novelties that evolved into a functionally coherent motor control system in an almost stereotypic organization across vertebrate taxa.

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“…What is the ionic basis for the long-lasting, deep AHPs of regular units and the brief, shallow AHPs of irregular units? Most studies of this question have been done in bipolar cells of the vestibular ganglion (reviewed in Eatock et al 2008).…”

Section: Role Of Ionic Currents; Etiology Of Ahpsmentioning

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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Ion channels in mammalian vestibular afferents may set regularity of firing

Cited by 63 publications

References 85 publications

HCN Channels Expressed in the Inner Ear Are Necessary for Normal Balance Function

HCN Channels Expressed in the Inner Ear Are Necessary for Normal Balance Function

Connecting Ears to Eye Muscles: Evolution of a ‘Simple' Reflex Arc

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

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