Temporal plasticity in auditory cortex improves neural discrimination of speech sounds

Shetake, Jai A.; Vrana, Will A.; Wolf, Jordan T.; Kilgard, Michael P.

doi:10.1016/j.brs.2017.01.007

Cited by 10 publications

(8 citation statements)

References 63 publications

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“…Although previous studies have shown plasticity in A1 following VNS, most performed chronic pairing of VNS with sound presentation over many days, e.g., 300 times/day for 20 days Engineer et al (2015b); Shetake et al (2012); Engineer et al (2017, 2011); Borland et al (2019). Here, we studied short-term effects of VNS on auditory learning and cortical plasticity in A1.…”

Section: Introductionmentioning

confidence: 99%

Short-term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex

Lai

David

2019

Preprint

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2Chronic vagus nerve stimulation (VNS) can facilitate learning of sensory and motor behaviors. 3 VNS is believed to trigger release of neuromodulators, including norepinephrine and acetylcholine, 4 which can mediate cortical plasticity associated with learning. Most previous work has studied 5 effects of VNS over many days, and less is known about how acute VNS influences neural coding 6 and behavior over the shorter term. To explore this question, we measured effects of VNS on 7 learning of an auditory discrimination over 1-2 days. Ferrets implanted with cuff electrodes on 8 the vagus nerve were trained by classical conditioning on a tone frequency-reward association. 9 One tone was associated with reward while another tone, was not. The frequencies and reward 10 associations of the tones were changed every two days, requiring learning of a new relationship. 11 When the tones (both rewarded and non-rewarded) were paired with VNS, rates of learning 12 increased on the first day following a change in reward association. To examine VNS effects 13 on auditory coding, we recorded single-and multi-unit neural activity in primary auditory cortex 14 (A1) of passively listening animals following brief periods of VNS (20 trials/session) paired with 15 tones. Because afferent VNS induces changes in pupil size associated with fluctuations in 16 neuromodulation, we also measured pupil during recordings. After pairing VNS with a neuron's 17 1 Jesyin Lai Short-term VNSbest-frequency (BF) tone, responses in a subpopulation of neurons were reduced. Pairing with 18 an off-BF tone or performing VNS during the inter-trial interval had no effect on responses. 19 We separated the change in A1 activity into two components, one that could be predicted by 20 fluctuations in pupil and one that persisted after VNS and was not accounted for by pupil. The 21 BF-specific reduction in neural responses remained, even after regressing out changes that 22 could be explained by pupil. In addition, the size of VNS-mediated changes in pupil predicted the 23 magnitude of persistent changes in the neural response. This interaction suggests that changes 24 in neuromodulation associated with arousal gate the long-term effects of VNS on neural activity. 25 Taken together, these results support a role for VNS in auditory learning and help establish VNS 26 as a tool to facilitate neural plasticity. 27 28

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Section: Introductionmentioning

confidence: 99%

Short-term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex

Lai

David

2019

Preprint

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“…Inability of noiseexposed rats to detect silent gaps in narrow-band noise centered on the assumed tinnitus frequency was taken as a behavioral correlate of tinnitus; the gap impairment was eliminated after rats were continuously treated with VSN paired with tones excluding the frequency of tinnitus. To the best of our knowledge, all existing studies replicating these results are from the same group of authors (Shetake et al, 2012;Engineer et al, 2015Engineer et al, , 2017Buell et al, 2019;Adcock et al, 2020). No replication of this work by an independent research team exists.…”

Section: Discussionmentioning

confidence: 88%

“…VNS paired with tones could induce reorganization of the tonotopic map in the auditory cortex, enhancing cortical responses to the paired tone and altering the fields across the entire auditory pathway, increasing the percentage of each field that responds to the paired tone frequency (Engineer et al, 2011(Engineer et al, , 2015(Engineer et al, , 2017Shetake et al, 2012;Buell et al, 2019;Adcock et al, 2020).…”

Section: Vns: Targeting Plasticitymentioning

confidence: 99%

Direct and Transcutaneous Vagus Nerve Stimulation for Treatment of Tinnitus: A Scoping Review

Yakunina

Nam

2021

Front. Neurosci.

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Recent animal research has shown that vagus nerve stimulation (VNS) paired with sound stimuli can induce neural plasticity in the auditory cortex in a controlled manner. VNS paired with tones excluding the tinnitus frequency eliminated physiological and behavioral characteristics of tinnitus in noise-exposed rats. Several clinical trials followed and explored the effectiveness of VNS paired with sound stimuli for alleviating tinnitus in human subjects. Transcutaneous VNS (tVNS) has received increasing attention as a non-invasive alternative approach to tinnitus treatment. Several studies have also explored tVNS alone (not paired with sound stimuli) as a potential therapy for tinnitus. In this review, we discuss existing knowledge about direct and tVNS in terms of applicability, safety, and effectiveness in diminishing tinnitus symptoms in human subjects. This review includes all existing clinical and neuroimaging studies of tVNS alone or paired with acoustic stimulation in tinnitus patients and outlines the present limitations that must be overcome to maximize the potential of (t)VNS as a therapy for tinnitus.

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“…These effects can generalize across stimuli. After pairing tone trains at rapid 15 pulse/s with VNS, A1 responses were also increased for unpaired novel speech sounds ( Engineer et al, 2017 ). It has also been demonstrated that VNS modulates synchrony and excitability in the A1 at least in part through the activation of muscarinic acetylcholine receptors ( Nichols et al, 2011 ).…”

Section: Discussionmentioning

confidence: 99%

“…Most previous studies of VNS-mediated plasticity in the auditory system have measured plasticity following chronic VNS, e.g., 300 times/d for 20 d ( Engineer et al, 2011 , 2015 , 2017 ; Shetake et al, 2012 ; Borland et al, 2019 ). Here, short-term effects of VNS on auditory learning and cortical plasticity were explored.…”

Section: Introductionmentioning

confidence: 99%

Short-Term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex

Lai

David

2021

eNeuro

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Chronic vagus nerve stimulation (VNS) has been shown to facilitate learning, but effects of acute VNS on neural coding and behavior remain less well understood. Ferrets implanted with cuff electrodes on the vagus nerve were trained by classical conditioning on an auditory tone frequency-reward association. One tone was associated with reward while another tone was not. Tone frequencies and reward associations were changed every 2 days, requiring learning of a new relationship. When tones were paired with VNS, animals consistently learned the new association within 2 days. When VNS occurred randomly between trials, learning within 2 days was unreliable. In passively listening animals, neural activity in primary auditory cortex and pupil size were recorded before and after acute VNS-tone pairing.After pairing with a neuron's best-frequency (BF) tone, responses by a subpopulation of neurons were reduced. VNS paired with an off-BF tone or during inter-trial intervals had no effect. The BF-specific reduction in neural responses after VNS remained, even after regressing out changes explained by pupil-indexed arousal. VNS induced brief dilation in the pupil, and the size of this change predicted the magnitude of persistent changes in the neural response. This interaction suggests that fluctuations in neuromodulation associated with arousal gate the long-term VNS effects on neural activity.

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Temporal plasticity in auditory cortex improves neural discrimination of speech sounds

Cited by 10 publications

References 63 publications

Short-term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex

Short-term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex

Direct and Transcutaneous Vagus Nerve Stimulation for Treatment of Tinnitus: A Scoping Review

Short-Term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex

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