Hyperactivity following unilateral hearing loss in characterized cells in the inferior colliculus

Vogler, Darryl P.; Robertson, Donald; Mulders, Wilhelmina

doi:10.1016/j.neuroscience.2014.01.017

Cited by 35 publications

(40 citation statements)

References 53 publications

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“…And finally, in the present study, in people with tinnitus and/or low sound tolerance, we found elevated responsiveness of the MOC system, which involves neuronal types in yet another division of the cochlear nucleus, the PVCN. In other words, there is evidence for hyperactivity and/or hyperresponsiveness associated with tinnitus and low sound tolerance in structures ranging from the cochlea (efferent feedback; present study) to inferior colliculus (Bauer et al 2008;Gu et al 2010;Vogler et al 2014) and in neural pathways distributed across every major division of the cochlear nucleus, the source of all ascending signals in the central auditory pathway. We propose that hyperactivity/hyperresponsiveness is ubiquitous in the auditory brain stem of people with tinnitus and/or low sound tolerance.…”

Section: Discussionmentioning

confidence: 49%

Increased contralateral suppression of otoacoustic emissions indicates a hyperresponsive medial olivocochlear system in humans with tinnitus and hyperacusis

Knudson

Shera

Melcher

2014

Journal of Neurophysiology

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Knudson IM, Shera CA, Melcher JR. Increased contralateral suppression of otoacoustic emissions indicates a hyperresponsive medial olivocochlear system in humans with tinnitus and hyperacusis. J Neurophysiol 112: 3197-3208, 2014. First published September 17, 2014 doi:10.1152/jn.00576.2014.-Atypical medial olivocochlear (MOC) feedback from brain stem to cochlea has been proposed to play a role in tinnitus, but even well-constructed tests of this idea have yielded inconsistent results. In the present study, it was hypothesized that low sound tolerance (mild to moderate hyperacusis), which can accompany tinnitus or occur on its own, might contribute to the inconsistency. Sound-level tolerance (SLT) was assessed in subjects (all men) with clinically normal or near-normal thresholds to form threshold-, age-, and sex-matched groups: 1) no tinnitus/high SLT, 2) no tinnitus/low SLT, 3) tinnitus/high SLT, and 4) tinnitus/low SLT. MOC function was measured from the ear canal as the change in magnitude of distortion-product otoacoustic emissions (DPOAE) elicited by broadband noise presented to the contralateral ear. The noise reduced DPOAE magnitude in all groups ("contralateral suppression"), but significantly more reduction occurred in groups with tinnitus and/or low SLT, indicating hyperresponsiveness of the MOC system compared with the group with no tinnitus/high SLT. The results suggest hyperresponsiveness of the interneurons of the MOC system residing in the cochlear nucleus and/or MOC neurons themselves. The present data, combined with previous human and animal data, indicate that neural pathways involving every major division of the cochlear nucleus manifest hyperactivity and/or hyperresponsiveness in tinnitus and/or low SLT. The overactivation may develop in each pathway separately. However, a more parsimonious hypothesis is that top-down neuromodulation is the driving force behind ubiquitous overactivation of the auditory brain stem and may correspond to attentional spotlighting on the auditory domain in tinnitus and hyperacusis.

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Section: Discussionmentioning

confidence: 49%

Increased contralateral suppression of otoacoustic emissions indicates a hyperresponsive medial olivocochlear system in humans with tinnitus and hyperacusis

Knudson

Shera

Melcher

2014

Journal of Neurophysiology

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“…A more complete description on the effects of noise trauma on the spontaneous firing in IC has been published elsewhere (Mulders and Robertson 2009, 2011Vogler et al 2014). Ninety-five percent of units in IC have a low spontaneous firing rate (Ͻ8 spikes/s) in normal animals (Mulders and Robertson 2009).…”

Section: Resultsmentioning

confidence: 99%

“…As tinnitus is associated with hearing loss in most, if not all, cases (Chung et al 1984;Sindhusake et al 2003), hearing loss has been suggested to act as a necessary cause or trigger of tinnitus. Many studies have shown that hearing loss is accompanied by both spontaneous and stimulus-induced hyperactivity at different levels of the central auditory system, i.e., the cochlear nucleus (Bledsoe et al 2009;Kaltenbach and Afman 2000;Sumner et al 2005;Vogler et al 2011), the inferior colliculus (IC) (Bauer et al 2008;Izquierdo et al 2008;Robertson 2009, 2011;Vogler et al 2014) and the auditory cortex (Komiya and Eggermont 2000;Noreña et al 2010;Eggermont 2003, 2006;Seki and Eggermont 2003). This increase in central neural activity occurs despite the reduction of spontaneous and stimulusevoked cochlear nerve activity after cochlear lesions (Hartmann et al 1984;Heinz and Young 2004;Kujawa and Liberman 2009;Liberman and Dodds 1984;Shepherd and Javel 1997).…”

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confidence: 99%

Suppression of putative tinnitus-related activity by extra-cochlear electrical stimulation

Noreña

Mulders

Robertson

2015

Journal of Neurophysiology

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Noreña AJ, Mulders WH, Robertson D. Suppression of putative tinnitus-related activity by extra-cochlear electrical stimulation. J Neurophysiol 113: 132-143, 2015. First published October 8, 2014 doi:10.1152/jn.00580.2014.-Studies on animals have shown that noise-induced hearing loss is followed by an increase of spontaneous firing at several stages of the central auditory system. This central hyperactivity has been suggested to underpin the perception of tinnitus. It was shown that decreasing cochlear activity can abolish the noise-induced central hyperactivity. This latter result further suggests that an approach consisting of reducing cochlear activity may provide a therapeutic avenue for tinnitus. In this context, extra-cochlear electric stimulation (ECES) may be a good candidate to modulate cochlear activity and suppress tinnitus. Indeed, it has been shown that a positive current applied at the round window reduces cochlear nerve activity and can suppress tinnitus reliably in tinnitus subjects. The present study investigates whether ECES with a positive current can abolish the noise-induced central hyperactivity, i.e., the putative tinnitus-related activity. Spontaneous and stimulus-evoked neural activity before, during and after ECES was assessed from single-unit recordings in the inferior colliculus of anesthetized guinea pigs. We found that ECES with positive current significantly decreases the spontaneous firing rate of neurons with high characteristic frequencies, whereas negative current produces the opposite effect. The effects of the ECES are absent or even reversed for neurons with low characteristic frequencies. Importantly, ECES with positive current had only a marginal effect on thresholds and tone-induced activity of collicular neurons, suggesting that the main action of positive current is to modulate the spontaneous firing. Overall, cochlear electrical stimulation may be a viable approach for suppressing some forms of (peripheral-dependent) tinnitus.

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“…Recent studies have described hyperactivity in the ICC of guinea pigs using alternative physiological classifications (Vogler et al 2014). Neurons with monaural rate-level functions showed a statistically significant increase in spontaneous activity after sound exposure.…”

Section: Role Of the Vcnmentioning

confidence: 99%

“…Although this study presents indirect evidence for the transformation of type I units into tail units, future studies may gain important insights into the mechanisms of tinnitus induction from a more detailed functional segregation that is based on empirical confirmation of their brainstem inputs. Based on the results of Vogler et al (2014), further refinements in the classification of type I units are also warranted.…”

Section: Considerations For Future Studiesmentioning

confidence: 99%

Effects of Unilateral Acoustic Trauma on Tinnitus-Related Spontaneous Activity in the Inferior Colliculus

Ropp

Tiedemann

Young

et al. 2014

JARO

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This study describes the long-term effects of soundinduced cochlear trauma on spontaneous discharge rates in the central nucleus of the inferior colliculus (ICC). As in previous studies, single-unit recordings in Sprague-Dawley rats revealed pervasive increases in spontaneous discharge rates. Based on differences in their sources of input, it was hypothesized that physiologically defined neural populations of the auditory midbrain would reveal the brainstem sources that dictate ICC hyperactivity. Abnormal spontaneous activity was restricted to target neurons of the ventral cochlear nucleus. Nearly identical patterns of hyperactivity were observed in the contralateral and ipsilateral ICC. The elevation in spontaneous activity extended to frequencies well below and above the region of maximum threshold shift. This lack of frequency organization suggests that ICC hyperactivity may be influenced by regions of the brainstem that are not tonotopically organized. Sound-induced hyperactivity is often observed in animals with behavioral signs of tinnitus. Prior to electrophysiological recording, rats were screened for tinnitus by measuring gap pre-pulse inhibition of the acoustic startle reflex (GPIASR). Rats with positive phenotypes did not exhibit unique patterns of ICC hyperactivity. This ambiguity raises concerns regarding animal behavioral models of tinnitus. If our screening procedures were valid, ICC hyperactivity is observed in animals without behavioral indications of the disorder. Alternatively, if the perception of tinnitus is strictly linked to ongoing ICC hyperactivity, our current behavioral approach failed to provide a reliable assessment of tinnitus state.

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Hyperactivity following unilateral hearing loss in characterized cells in the inferior colliculus

Cited by 35 publications

References 53 publications

Increased contralateral suppression of otoacoustic emissions indicates a hyperresponsive medial olivocochlear system in humans with tinnitus and hyperacusis

Increased contralateral suppression of otoacoustic emissions indicates a hyperresponsive medial olivocochlear system in humans with tinnitus and hyperacusis

Suppression of putative tinnitus-related activity by extra-cochlear electrical stimulation

Effects of Unilateral Acoustic Trauma on Tinnitus-Related Spontaneous Activity in the Inferior Colliculus

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