The Corticofugal Effects of Auditory Cortex Microstimulation on Auditory Nerve and Superior Olivary Complex Responses Are Mediated via Alpha-9 Nicotinic Receptor Subunit

Aedo, Cristián; Terreros, Gonzalo; León, Alex; Délano, Paul H.

doi:10.1371/journal.pone.0155991

Cited by 16 publications

(18 citation statements)

References 37 publications

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“…Evidences in bats [34] and chinchillas [35, 36] have demonstrated that the inactivation and electrical stimulation of the auditory cortex can modulate cochlear responses in a frequency specific manner. In addition, Aedo et al [37] showed in the alpha-9 nicotinic receptor knock-out mice that these corticofugal effects are produced through the medial olivocochlear system.…”

Section: Discussionmentioning

confidence: 99%

Oscillatory infrasonic modulation of the cochlear amplifier by selective attention

et al. 2019

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Evidence shows that selective attention to visual stimuli modulates the gain of cochlear responses, probably through auditory-cortex descending pathways. At the cerebral cortex level, amplitude and phase changes of neural oscillations have been proposed as a correlate of selective attention. However, whether sensory receptors are also influenced by the oscillatory network during attention tasks remains unknown. Here, we searched for oscillatory attention-related activity at the cochlear receptor level in humans. We used an alternating visual/auditory selective attention task and measured electroencephalographic activity simultaneously to distortion product otoacoustic emissions (a measure of cochlear receptor-cell activity). In order to search for cochlear oscillatory activity, the otoacoustic emission signal, was included as an additional channel in the electroencephalogram analyses. This method allowed us to evaluate dynamic changes in cochlear oscillations within the same range of frequencies (1–35 Hz) in which cognitive effects are commonly observed in electroencephalogram works. We found the presence of low frequency (<10 Hz) brain and cochlear amplifier oscillations during selective attention to visual and auditory stimuli. Notably, switching between auditory and visual attention modulates the amplitude and the temporal order of brain and inner ear oscillations. These results extend the role of the oscillatory activity network during cognition in neural systems to the receptor level.

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Section: Discussionmentioning

confidence: 99%

Oscillatory infrasonic modulation of the cochlear amplifier by selective attention

et al. 2019

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“…The auditory efferent system is a neural network that comprises descending projections from the auditory cortex to the inferior colliculus, cochlear nucleus and superior olivary complex 10 – 12 , from where the medial olivocochlear (MOC) bundle emerges making synapses directly with outer hair cells of the cochlea 13 . The functionality of these corticofugal pathways has been demonstrated in bats, chinchillas and humans 14 – 17 , and these descending projections are proposed to be the mediators of selective attention top-down effects on the cochlear receptor 18 , 19 . In addition, peripheral modulations of the cochlear receptor during visual attention have been demonstrated in humans 20 – 22 .…”

Section: Introductionmentioning

confidence: 99%

The olivocochlear reflex strength in awake chinchillas is relevant for behavioural performance during visual selective attention with auditory distractors

Bowen

Terreros

Moreno‐Gómez

et al. 2020

Sci Rep

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The auditory efferent system comprises descending projections from the cerebral cortex to subcortical nuclei, reaching the cochlear receptor through olivocochlear fibres. One of the functions attributed to this corticofugal system is to suppress irrelevant sounds during selective attention to visual stimuli. Medial olivocochlear neurons can also be activated by sounds through a brainstem reflex circuit. Whether the individual variability of this reflex is related to the cognitive capacity to suppress auditory stimuli is still controversial. Here we propose that the individual strength per animal of the olivocochlear reflex is correlated with the ability to suppress auditory distractors during visual attention in awake chinchillas. The olivocochlear reflex was elicited with a contralateral broad-band noise at ~ 60 dB and ipsilateral distortion product otoacoustic emissions were obtained at different frequencies (1–8 kHz). Fourteen chinchillas were evaluated in a behavioural protocol of visual attention with broad-band noise and chinchilla vocalizations as auditory distractors. Results show that the behavioural performance was affected by both distractors and that the magnitudes of the olivocochlear reflex evaluated at multiple frequencies were relevant for behavioural performance during visual discrimination with auditory distractors. These results stress the ecological relevance of the olivocochlear system for suppressing natural distractors.

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“…The significant increase of early incorrect responses could be indicative of more impulsive decision in KO mice induced by auditory distraction in a visual selective attention task. Auditory-cortex descending pathways can be though as a neural circuit that allows top-down filtering of afferent auditory responses (Xiao and Suga, 2002 ; León et al, 2012 ; Aedo et al, 2016 ). In that line, we propose that the increased auditory distraction in KO mice could be consequence of the lack of OHC inhibition by MOC synapses in the KO mice.…”

Section: Discussionmentioning

confidence: 99%

“…In that line, we propose that the increased auditory distraction in KO mice could be consequence of the lack of OHC inhibition by MOC synapses in the KO mice. This might impair the filtering of auditory distractors by the corticofugal projections from the auditory cortex that modulate MOC neurons (Dragicevic et al, 2015 ; Aedo et al, 2016 ). Importantly, auditory thresholds and supra-thresholds ABR amplitudes were similar for WT and KO mice, and only a significant difference in the latency of wave V was obtained.…”

Section: Discussionmentioning

confidence: 99%

Difference in Perseverative Errors during a Visual Attention Task with Auditory Distractors in Alpha-9 Nicotinic Receptor Subunit Wild Type and Knock-Out Mice

Jorratt

Délano

Delgado

et al. 2017

Front. Cell. Neurosci.

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The auditory efferent system is a neural network that originates in the auditory cortex and projects to the cochlear receptor through olivocochlear (OC) neurons. Medial OC neurons make cholinergic synapses with outer hair cells (OHCs) through nicotinic receptors constituted by α9 and α10 subunits. One of the physiological functions of the α9 nicotinic receptor subunit (α9-nAChR) is the suppression of auditory distractors during selective attention to visual stimuli. In a recent study we demonstrated that the behavioral performance of alpha-9 nicotinic receptor knock-out (KO) mice is altered during selective attention to visual stimuli with auditory distractors since they made less correct responses and more omissions than wild type (WT) mice. As the inhibition of the behavioral responses to irrelevant stimuli is an important mechanism of the selective attention processes, behavioral errors are relevant measures that can reflect altered inhibitory control. Errors produced during a cued attention task can be classified as premature, target and perseverative errors. Perseverative responses can be considered as an inability to inhibit the repetition of an action already planned, while premature responses can be considered as an index of the ability to wait or retain an action. Here, we studied premature, target and perseverative errors during a visual attention task with auditory distractors in WT and KO mice. We found that α9-KO mice make fewer perseverative errors with longer latencies than WT mice in the presence of auditory distractors. In addition, although we found no significant difference in the number of target error between genotypes, KO mice made more short-latency target errors than WT mice during the presentation of auditory distractors. The fewer perseverative error made by α9-KO mice could be explained by a reduced motivation for reward and an increased impulsivity during decision making with auditory distraction in KO mice.

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The Corticofugal Effects of Auditory Cortex Microstimulation on Auditory Nerve and Superior Olivary Complex Responses Are Mediated via Alpha-9 Nicotinic Receptor Subunit

Cited by 16 publications

References 37 publications

Oscillatory infrasonic modulation of the cochlear amplifier by selective attention

Oscillatory infrasonic modulation of the cochlear amplifier by selective attention

The olivocochlear reflex strength in awake chinchillas is relevant for behavioural performance during visual selective attention with auditory distractors

Difference in Perseverative Errors during a Visual Attention Task with Auditory Distractors in Alpha-9 Nicotinic Receptor Subunit Wild Type and Knock-Out Mice

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