scholarly journals Hair-Cell Versus Afferent Adaptation in the Semicircular Canals

2005 ◽  
Vol 93 (1) ◽  
pp. 424-436 ◽  
Author(s):  
R. D. Rabbitt ◽  
R. Boyle ◽  
G. R. Holstein ◽  
S. M. Highstein

The time course and extent of adaptation in semicircular canal hair cells was compared to adaptation in primary afferent neurons for physiological stimuli in vivo to study the origins of the neural code transmitted to the brain. The oyster toadfish, Opsanus tau, was used as the experimental model. Afferent firing-rate adaptation followed a double-exponential time course in response to step cupula displacements. The dominant adaptation time constant varied considerably among afferent fibers and spanned six orders of magnitude for the population (∼1 ms to >1,000 s). For sinusoidal stimuli (0.1–20 Hz), the rapidly adapting afferents exhibited a 90° phase lead and frequency-dependent gain, whereas slowly adapting afferents exhibited a flat gain and no phase lead. Hair-cell voltage and current modulations were similar to the slowly adapting afferents and exhibited a relatively flat gain with very little phase lead over the physiological bandwidth and dynamic range tested. Semicircular canal microphonics also showed responses consistent with the slowly adapting subset of afferents and with hair cells. The relatively broad diversity of afferent adaptation time constants and frequency-dependent discharge modulations relative to hair-cell voltage implicate a subsequent site of adaptation that plays a major role in further shaping the temporal characteristics of semicircular canal afferent neural signals.

2000 ◽  
Vol 83 (5) ◽  
pp. 2740-2756 ◽  
Author(s):  
S. Masetto ◽  
P. Perin ◽  
A. Malusà ◽  
G. Zucca ◽  
P. Valli

The electrophysiological properties of developing vestibular hair cells have been investigated in a chick crista slice preparation, from embryonic day 10 ( E10) to E21 (when hatching would occur). Patch-clamp whole-cell experiments showed that different types of ion channels are sequentially expressed during development. An inward Ca2+ current and a slow outward rectifying K+current ( I K(V)) are acquired first, at or before E10, followed by a rapid transient K+current ( I K(A)) at E12, and by a small Ca-dependent K+ current ( I KCa) at E14. Hair cell maturation then proceeds with the expression of hyperpolarization-activated currents: a slow I h appears first, around E16, followed by the fast inward rectifier I K1around E19. From the time of its first appearance, I K(A) is preferentially expressed in peripheral ( zone 1) hair cells, whereas inward rectifying currents are preferentially expressed in intermediate ( zone 2) and central ( zone 3) hair cells. Each conductance conferred distinctive properties on hair cell voltage response. Starting from E15, some hair cells, preferentially located at the intermediate region, showed the amphora shape typical of type I hair cells. From E17 (a time when the afferent calyx is completed) these cells expressed I K, L, the signature current of mature type I hair cells. Close to hatching, hair cell complements and regional organization of ion currents appeared similar to those reported for the mature avian crista. By the progressive acquisition of different types of inward and outward rectifying currents, hair cell repolarization after both positive- and negative-current injections is greatly strengthened and speeded up.


2009 ◽  
Vol 102 (3) ◽  
pp. 1513-1525 ◽  
Author(s):  
Richard Boyle ◽  
Richard D. Rabbitt ◽  
Stephen M. Highstein

The sensations of sound and motion generated by the inner ear are controlled by the brain through extensive centripetal innervation originating within the brain stem. In the semicircular canals, brain stem efferent neurons make synaptic contacts with mechanosensory hair cells and with the dendrites of afferent neurons. Here, we examine the relative contributions of efferent action on hair cells and afferents. Experiments were performed in vivo in the oyster toadfish, Opsanus tau. The efferent system was activated via electrical pulses to the brain stem and sensory responses to motion stimuli were quantified by simultaneous voltage recording from afferents and intracellular current- and/or voltage-clamp recordings from hair cells. Results showed synaptic inputs to both afferents and hair cells leading to relatively long-latency intracellular signaling responses: excitatory in afferents and inhibitory in hair cells. Generally, the net effect of efferent action was an increase in afferent background discharge and a simultaneous decrease in gain to angular motion stimuli. Inhibition of hair cells was likely the result of a ligand-gated opening of a major basolateral conductance. The reversal potential of the efferent-evoked current was just below the hair cell resting potential, thus resulting in a small hyperpolarization. The onset latency averaged about 90 ms and latency to peak response was 150–400 ms. Hair cell inhibition often outlasted afferent excitation and, in some cases, latched hair cells in the “off” condition for >1 s following cessation of stimulus. These features endow the animal with a powerful means to adjust the sensitivity and dynamic range of motion sensation.


2016 ◽  
Vol 28 (6) ◽  
pp. 811-823 ◽  
Author(s):  
Bryan S Joyce ◽  
Pablo A Tarazaga

The cochlea displays an important, nonlinear amplification of sound-induced oscillations. In mammals, this amplification is largely powered by the somatic motility of the outer hair cells. The resulting cochlear amplifier has three important characteristics useful for hearing: an amplification of responses from low sound pressures, an improvement in frequency selectivity, and an ability to transduce a broad range of sound pressure levels. These useful features can be incorporated into designs for active artificial hair cells, bio-inspired sensors for use as microphones, accelerometers, or other dynamic sensors. The sensor consists of a cantilever beam with piezoelectric actuators. A feedback controller applies a voltage to the actuators to mimic the outer hair cells’ somatic motility. This article describes three control laws for an active artificial hair cell inspired by models of the outer hair cells’ somatic motility. The first control law is based on a phenomenological model of the cochlea while the second and third models incorporate physiological aspects of the biological cochlea to further improve sensor performance. Simulations show that these models qualitatively reproduce the key aspects of the mammalian cochlea, namely, amplification of oscillations from weak stimuli, higher quality factors, and a wider input dynamic range.


Cephalalgia ◽  
2008 ◽  
Vol 28 (6) ◽  
pp. 631-639 ◽  
Author(s):  
J Coste ◽  
DL Voisin ◽  
P Luccarini ◽  
R Dallel

Wind-up is a progressive, frequency-dependent increase in the excitability of trigeminal and spinal dorsal horn wide dynamic range (WDR) nociceptive neurons evoked by repetitive stimulation of primary afferent nociceptive C-fibres. The correlate of wind-up in humans is temporal summation, which is an increase in pain perception to repetitive constant nociceptive stimulation. Although wind-up is widely used as a tool for studying the processing of nociceptive information, including central sensitization, its actual role is still unknown. Here, we recorded from trigeminal WDR neurons using in vivo electrophysiological techniques in rats and assessed the wind-up phenomenon in response to stimuli of different intensities and frequencies. First, we found that the amplitude of C-evoked responses of WDR neurons to repetitive stimulation increased progressively to reach a peak, then consistently showed a stable or slightly decreasing plateau phase. Only the first phase of this time course fitted in with the wind-up description. Therefore, to assess wind-up, we measured a limited number of initial responses. Second, we showed that wind-up, i.e. the slope of the frequency-dependent increase in the response to C-fibre stimulation, was linearly correlated to the stimulus intensity. Intensities of brief C-fibre inputs were thus coded into frequencies of action potentials by second-order neurons through frequency-dependent potentiation of the evoked responses. Third, wind-up also occurred at stimulation intensities below the threshold for C-evoked responses in WDR neurons, suggesting that wind-up can amplify subthreshold C-fibre inputs to WDR neurons. This might account for the observation that sparse, subliminal, neuronal activity in nociceptors can become painful via central integration of neural responses. Altogether, the present results show that wind-up can provide trigeminal WDR neurons with the capability to encode the intensity of short-duration orofacial nociceptive stimuli and to detect subthreshold nociceptive input. Thus, not only may wind-up play a physiological role in trigeminal sensory processing, but its enhancement may also underlie the pathophysiology of chronic orofacial pain conditions.


1996 ◽  
Vol 76 (3) ◽  
pp. 1870-1879 ◽  
Author(s):  
Y. Kataoka ◽  
H. Ohmori

1. Experiments were performed to identify the excitatory amino acid (EAA) released from cochlear hair cells isolated from chick. An isolated hair cell was transported and closely apposed to a cultured granule cell or a Purkinje cell, and current responses were studied in these cell pairs when the apposed hair cell was depolarized. 2. The apposed hair cell was voltage clamped at -65 mV by a nystatin perforated-patch recording technique and the membrane potential was step changed to -10 or 0 mV to induce a release of neurotransmitter. In the granule cell voltage clamped at +55 mV, the hair cell membrane depolarization induced outward currents through the activation of the N-methyl-D-aspartate subtype of glutamate receptors. In the Purkinje cell voltage clamped at -60 mV, however, the hair cell depolarization could not induce any current responses. 3. Concentration-response relations for three endogenous EAAs (L-glutamate, L-aspartate, and L-homocysteate) were studied in the granule cell and in the Purkinje cell. The granule cell was most sensitive to glutamate, whereas these three EAAs did not show great sensitivity differences in the Purkinje cell and the half-maximum current was obtained at EAA concentrations of 17-60 microM. Concentrations of glutamate, aspartate, and homocysteate inducing the half-maximum current in the granule cell were 1.1, 11, and 10 microM, respectively. 4. The depolarization of the hair cell induced outward current (70 +/- 33 pA, mean +/- SD, n = 8) in the apposed granule cell voltage clamped at +55 mV. This current was equivalent to the current size induced by 0.33 microM glutamate, 5 microM aspartate, or 2 microM homocysteate. However, the critical concentration (0.33 microM) of glutamate failed to induce any current in the Purkinje cell voltage clamped at -60 mV. But the critical concentrations of the other two amino acids did evoke inward currents in the Purkinje cell. 5. These observations suggest that, of known neurotransmitter candidates, glutamate is the most likely to be released by cochlear hair cells in the chick. 6. Purkinje cells had an EAA-induced current that was not suppressed by 2-amino-5-phosphonovalerate (200 microM) or by 6-cyano-7-nitroquinoxaline-2,3-dione (20 microM). The current was dominant at low concentrations of EAAs (approximately 1.0 microM). This EAA-induced current was Na+ dependent and was likely carried through the high-affinity EAA transporter.


2019 ◽  
Author(s):  
Giusy A. Caprara ◽  
Andrew A. Mecca ◽  
Yanli Wang ◽  
Anthony J. Ricci ◽  
Anthony W. Peng

AbstractSound detection in auditory sensory hair cells depends on the deflection of the stereocilia hair bundle, which opens mechano-electric transduction (MET) channels. Adaptation is hypothesized to be a critical property of MET that contributes to the wide dynamic range and sharp frequency selectivity of the auditory system. Historically, adaptation was hypothesized to have multiple mechanisms, all of which require calcium entry through MET channels. Our recent work using a stiff probe to displace hair bundles showed that the fastest adaptation mechanism (fast adaptation) does not require calcium entry. Using a fluid-jet stimulus, others obtained data showing only a calcium-dependent fast adaptation response. Here, we identified the source of this discrepancy. Because the hair cell response to a hair bundle stimulus depends critically on the magnitude and time course of the hair bundle deflection, we developed a high-speed imaging technique to quantify this deflection. The fluid jet delivers a force stimulus, and step-like force stimuli lead to a complex time course of hair bundle displacement (mechanical creep), which affects the hair cell’s macroscopic MET current response by masking the time course of the fast adaptation response. Modifying the fluid-jet stimulus to generate a step-like hair bundle displacement produced rapidly adapting currents that did not depend on membrane potential. This indicated that fast adaptation does not depend on calcium entry. We also confirmed the presence of a calcium-dependent slow adaptation process. These results confirm the existence of multiple adaptation processes: a fast adaptation that is not driven by calcium entry and a slower calcium-dependent process.Significance StatementMechanotransduction by sensory hair cells represents a key first step for the sound sensing ability in vertebrates. The sharp frequency tuning and wide dynamic range of sound sensation are hypothesized to require a mechanotransduction adaptation mechanism. For decades, it had been accepted that all adaptation mechanisms require calcium entry into hair cells. However, more recent work indicated that the apparent calcium dependence of the fastest adaptation differs with the method of cochlear hair cell stimulation. Here, we reconcile existing data and show that calcium entry does not drive the fastest adaptation process, independent of the stimulation method.


2009 ◽  
Vol 101 (6) ◽  
pp. 2961-2973 ◽  
Author(s):  
Andrea Lelli ◽  
Yukako Asai ◽  
Andrew Forge ◽  
Jeffrey R. Holt ◽  
Gwenaëlle S. G. Géléoc

Inner ear hair cells are exquisite mechanosensors that transduce nanometer scale deflections of their sensory hair bundles into electrical signals. Several essential elements must be precisely assembled during development to confer the unique structure and function of the mechanotransduction apparatus. Here we investigated the functional development of the transduction complex in outer hair cells along the length of mouse cochlea acutely excised between embryonic day 17 (E17) and postnatal day 8 (P8). We charted development of the stereociliary bundle using scanning electron microscopy; FM1-43 uptake, which permeates hair cell transduction channels, mechanotransduction currents evoked by rapid hair bundle deflections, and mRNA expression of possible components of the transduction complex. We demonstrated that uptake of FM1-43 first occurred in the basal portion of the cochlea at P0 and progressed toward the apex over the subsequent week. Electrophysiological recordings obtained from 234 outer hair cells between E17 and P8 from four cochlear regions revealed a correlation between the pattern of FM1-43 uptake and the acquisition of mechanotransduction. We found a spatiotemporal gradient in the properties of transduction including onset, amplitude, operating range, time course, and extent of adaptation. We used quantitative RT–PCR to examine relative mRNA expression of several hair cell myosins and candidate tip-link molecules. We found spatiotemporal expression patterns for mRNA that encodes cadherin 23, protocadherin 15, myosins 3a, 7a, 15a, and PMCA2 that preceded the acquisition of transduction. The spatiotemporal expression patterns of myosin 1c and PMCA2 mRNA were correlated with developmental changes in several properties of mechanotransduction.


Author(s):  
Bryan S. Joyce ◽  
Pablo A. Tarazaga

Artificial hair cells (AHCs) are sensors inspired by biological hair cells. These devices often have lower sensitivities and poorer frequency resolutions than their biological counterparts. This is especially true when AHCs are placed in fluid. In the authors’ previous work, active AHCs were developed which used nonlinear feedback control to mimic the cochlea’s nonlinear amplifier. Incorporating this nonlinear control law can improve the AHC’s sensitivity, frequency selectivity, and dynamic range. This work examines an active artificial hair cell partially submerged in water. The fluid loading on the sensor adds inertia and significantly increases damping. A model of the sensor in air is developed and then modified to incorporate the added inertia and damping from the fluid. Simulation and experimental results show that the active artificial hair cell can overcome the added fluid inertia and damping to amplify oscillations due to low input levels and create a sharper frequency response. The resulting sensor is better suited to operate in fluid environments for flow sensing than an otherwise passive device. These sensors could potentially develop into replacements for damaged hair cells in the fluid-filled cochlea.


2005 ◽  
Vol 94 (5) ◽  
pp. 3134-3142 ◽  
Author(s):  
Andrei V. Derbenev ◽  
Cindy L. Linn ◽  
Paul S. Guth

In the frog, vestibular efferent fibers innervate only type-II vestibular hair cells. Through this direct contact with hair cells, efferent neurons are capable of modifying transmitter release from hair cells onto primary vestibular afferents. The major efferent transmitter, acetylcholine (ACh), is known to produce distinct pharmacological actions involving several ACh receptors. Previous studies have implicated the presence of muscarinic ACh receptors on vestibular hair cells, although, surprisingly, a muscarinic-mediated electrical response has not been demonstrated in solitary vestibular hair cells. This study demonstrates that muscarinic receptors can evoke transmitter release from vestibular hair cells. Detection of this release was obtained through patch-clamp recordings from catfish cone horizontal cells, serving as glutamate detectors after pairing them with isolated frog semicircular canal hair cells in a two-cell preparation. Although horizontal cells alone failed to respond to carbachol, application of 20 μM carbachol to the two-cell preparation resulted in a horizontal cell response that could be mimicked by exogenous application of glutamate. All of the horizontal cells in the two-cell preparation responded to 20 μM CCh. Furthermore, this presumed transmitter release persisted in the presence of d-tubocurarine at concentrations that block all known hair cell nicotinic ACh receptors. The effect on the detector cell, imparted by the carbachol application to the hair cell-horizontal cell preparation, was blocked both by 2-amino-5-phosphonopentanoic acid, a selective N-methyl-d-aspartate antagonist, and the muscarinic antagonist, atropine. Thus vestibular hair cells from the frog semicircular canal can be stimulated to release transmitter by activating their muscarinic receptors.


Author(s):  
Bryan S. Joyce ◽  
Pablo A. Tarazaga

There is interest in developing devices that mimic the sound transduction of the cochlear hair cells. Current artificial hair cell (AHC) designs have focused on passive transduction of sound into electrical signals. However, measurements inside living cochleae have revealed that a nonlinear amplification is at work in mammalian hearing. This amplification lowers the threshold for sound detection allowing mammals to hear faint sounds. The nonlinearity results in an amplitude compression whereby a large range of sound pressure levels produces a smaller range of displacements. This compressive nonlinearity gives the ear a large dynamic range. This work seeks to develop and analyze active artificial hair cells which employ a bio-inspired amplification to improve performance. This paper examines two artificial hair cell designs. The first is an 18.5 in long aluminum cantilever beam which is excited and controlled using piezoelectric actuators along the length of the beam. The second design is a one inch piezoelectric bimorph beam subject to a base excitation. In both cases a nonlinear feedback control law is implemented which reduces the beam’s linear viscous damping and introduces a cubic damping term. Model and experimental results show the control law amplified the response of the artificial hair cell to low excitation levels near the resonance frequency. Increasing input levels produced a compressive nonlinearity at resonance similar to that observed in measurements from mammalian cochleae. This work could lead to the development of new bio-inspired sensors with a lower threshold of detection, improved frequency sensitivity, and larger dynamic range.


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