Recovery of the compound action potential following prior stimulation: Evidence for a slow component that reflects recovery of low spontaneous-rate auditory neurons

Relkin, Evan M.; Doucet, John R.; Sterns, Anita

doi:10.1016/0378-5955(95)00004-n

Cited by 24 publications

(17 citation statements)

References 22 publications

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“…Our presynaptic measurements now show a slowing of the secretory rate of IHCs, most likely reflecting depletion of the RRP, with a time course ( ϭ 10 ms) compatible to the time courses of rapid and short-term adaptation. Moreover, we observed a biphasic time course for the RRP recovery from depletion, which was similar to that of the compound action potential recovery from adaptation in the auditory nerve (37). We therefore conclude that presynaptic depletion of release-ready vesicles may contribute to fast auditory adaptation.…”

Section: Ca 2ϩsupporting

confidence: 52%

Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse

Moser

Beutner

2000

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

392

561

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Hearing in mammals relies on the highly synchronous synaptic transfer between cochlear inner hair cells (IHCs) and the auditory nerve. We studied the presynaptic function of single mouse IHCs by monitoring membrane capacitance changes and voltage-gated Ca 2؉ currents. Exocytosis initially occurred at a high rate but then slowed down within a few milliseconds, despite nearly constant Ca 2؉ influx. We interpret the observed secretory depression as depletion of a readily releasable pool (RRP) of about 280 vesicles. These vesicles are probably docked close to Ca 2؉ channels at the ribbon-type active zones of the IHCs. Continued depolarization evoked slower exocytosis occurring at a nearly constant rate for at least 1 s and depending on ''long-distance'' Ca 2؉ signaling. Refilling of the RRP after depletion followed a biphasic time course and was faster than endocytosis. RRP depletion is discussed as a mechanism for fast auditory adaptation. influx at the ribbon-type active zones triggers exocytosis of synaptic vesicles, which probably release glutamate (2) onto glutamate receptors (3, 4) of the postsynaptic auditory nerve fibers. There is little information about the presynaptic function of IHCs, because the small diameter of auditory nerve fibers in mammals hinders postsynaptic recordings. Assumptions about transmitter release have, therefore, mainly been based on auditory nerve fiber spiking rate data (5) or on Furukawa's classical recordings of postsynaptic potentials from goldfish (6).To study the presynaptic function of mouse IHCs independently of postsynaptic recordings, we detected the exocytic fusion and endocytic retrieval of synaptic vesicle membrane as changes of the membrane capacitance (C m ; ref. 7). The specificity of C m measurements for reporting exocytosis of neurotransmitters has recently been confirmed in another ribbon-type presynapse, that of the goldfish retinal bipolar nerve terminal, by simultaneously recording transmitter release (8). In these neurons, as well as in neuroendocrine cells, several kinetic components of exocytosis have been observed and attributed to release of functionally different pools of vesicles (9-12). We compare the presynaptic properties of IHCs to the findings in other neurosecretory preparations and discuss them in the context of auditory adaptation and recovery from adaptation. ] e ; 10 mM CaCl 2 ) was used for all experiments except for those of Fig. 1b (2 mM CaCl 2 ). The extracellular solution further contained (in mM) 105 NaCl, 35 tetraethylammonium chloride (Pfaltz & Bauer), 2.8 KCl, 1 MgCl 2 , 10 NaOH-Hepes, and 10 D-glucose (pH 7.2). Solution changes were achieved by bath exchange. IHCs were stimulated electrically rather than mechanically, because C m measurements require voltage clamp. Unless stated otherwise, a resting period of Ϸ30 s was kept between depolarizations to allow recovery of exocytosis. EPC-9 amplifiers (HEKA Electronics, Lambrecht͞Pfalz, Germany) controlled by PULSE software (HEKA Electronics) were used for measurements. All voltages were co...

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Section: Ca 2ϩsupporting

confidence: 52%

Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse

Moser

Beutner

2000

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

392

561

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“…A large number of animal studies on adaptation and/ or recovery of AN responses have been reported, most of which have involved eliciting responses from single units of the AN using a peristimulatory adaptation technique (Smith and Brachman, 1982;Westernman and Smith, 1984) or forward-masking protocols (Abbas and Gorga, 1981;Schreiner, 1990, 1991;Reklin and Doucet, 1991;Relkin et al, 1995;Smith, 1977) using noise or a pure tone as a masker. Relkin et al (1995) investigated the recovery process of the CAP in chinchillas using forward masking with an 8.0 kHz tone burst as the masker.…”

Section: Recovery Process Of the Capmentioning

confidence: 99%

“…Many animal experiments have investigated adaptation and/or recovery of AN responses using forwardmasking (Abbas and Gorga, 1981;Schreiner, 1990, 1991;Reklin and Doucet, 1991;Relkin et al, 1995), peristimulatory-masking (Smith and Brachman, 1982;Westernman and Smith, 1984) and pairedclick stimulation (Finck and Ruben, 1962;Parham et al, 1996Parham et al, , 1998 protocols. There are several reports on CAP recovery in humans as assessed using a forward-masking protocol (Coats and Dickey, 1972;Spoor et al, 1976;Murnane et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Recovery of human compound action potential using a paired-click stimulation paradigm

et al. 2005

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“…Presentations were 1 s apart. The normalized decremental response was calculated following the example of Relkin et al (1995):…”

Section: Physiological Proceduresmentioning

confidence: 99%

“…The number of fibers recorded in control and furosemidetreated animals ranged from four to 85 per animal, thus it is possible that sampling error or other unknown biases may be present in these single-fiber data. To further examine the activities of low-SR auditory nerve fibers after furosemide exposure, we employed a method developed by Relkin et al (1995) using the recovery from a prior conditioning stimulus of the auditory whole-nerve response, CAP response. The CAP is an evoked population response that can be free from the sampling errors that may be present in single-fiber recording procedures.…”

Section: Effect Of Furosemide On Cap Recovery Functionmentioning

confidence: 99%

Chronic Reduction of Endocochlear Potential Reduces Auditory Nerve Activity: Further Confirmation of an Animal Model of Metabolic Presbyacusis

Lang

Jyothi

Smythe

et al. 2010

JARO

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Gerbils aged in quiet show a decline of the endocochlear potential (EP) and elevated auditory nerve compound action potential (CAP) thresholds. However, establishing a direct relationship between an age-related reduction in the EP and changes in the activities of primary auditory neurons is difficult owing to the complexity of age-related histological changes in the cochlea. To address this issue, we developed a young gerbil model of "metabolic" presbyacusis that uses an osmotic pump to deliver furosemide into the round window niche for 7 days, resulting in a chronically reduced EP. In this model, the only major histopathologic changes were restricted to the hook region of the cochlea and consisted of loss of strial intermediate cells and massive edema in the lateral wall. The morphological and physiological evidence suggests that the cochlea can adapt to furosemide application over time. The morphology of spiral ganglion cells and hair cells appeared normal throughout the cochlea. CAP responses and EP values in this model are similar to those of quiet-aged ears. The spontaneous activity of single auditory fibers (n= 188) was assessed in 15 young gerbils treated with furosemide for 7 days. The percentage of recorded low-spontaneous rate (SR) fibers at characteristic frequencies (CFs)≥6 kHz was significantly lower in furosemide-treated than in control ears. Recovery function tests of CAP responses after prior stimulation also showed a decline in activity of the low-SR population with CFs≥6 kHz in the treated cochleas. A similar loss in the activity of low-SR fiber has been previously shown in quiet-aged gerbils. These results suggest that dysfunction of the cochlear lateral wall and subsequent chronic reduction in the EP can directly affect the activity patterns of primary auditory neurons in a manner similar to that seen in aged gerbils.

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Recovery of the compound action potential following prior stimulation: Evidence for a slow component that reflects recovery of low spontaneous-rate auditory neurons

Cited by 24 publications

References 22 publications

Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse

Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse

Recovery of human compound action potential using a paired-click stimulation paradigm

Chronic Reduction of Endocochlear Potential Reduces Auditory Nerve Activity: Further Confirmation of an Animal Model of Metabolic Presbyacusis

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