Stimulus-Timing Dependent Multisensory Plasticity in the Guinea Pig Dorsal Cochlear Nucleus

Koehler, Seth D.; Shore, Susan E.

doi:10.1371/journal.pone.0059828

Cited by 47 publications

(77 citation statements)

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“…Timing rules from that in vivo study reflected recordings found in vitro (Tzounopoulos et al 2004), suggesting that bimodal stimulus timing-dependent plasticity in DCN neurons reflects STDP. In 40% of DCN units from sham-controls that exhibited stimulus timing dependency, auditory responses were facilitated after bimodal pairing in which Sp5 stimulation preceded tones but was suppressed if tones preceded Sp5 stimulation, thus exhibiting primarily Hebbian-like timing rules (Koehler and Shore 2013a). These results are consistent with the present findings in A1 sham-controls suggesting consistent mechanisms from brain stem to cortex.…”

Section: Discussionsupporting

confidence: 91%

“…Extracellular in vivo A1 single-unit responses to tones and SFRs measured before and after bimodal stimulation (paired Sp5-tone) demonstrated stimulus timing dependence similar to that shown in DCN for sham-controls (Koehler and Shore 2013a). Furthermore toneevoked bimodal plasticity timing rules were altered following noise-induced tinnitus: they were more likely to be Hebbian in sham-control animals and anti-Hebbian-like and enhancing in noise-exposed animals with tinnitus (ET), and somewhere in between in animals without tinnitus (ENT).…”

Section: Discussionmentioning

confidence: 57%

“…The present study tested the hypothesis that stimulus timingdependent plasticity as observed in DCN (Koehler and Shore 2013a) following bimodal stimulation is also observed in A1, and that it is modified following noise damage (Koehler and Shore 2013b). In A1, bimodal stimulation in sham-animals resulted in stimulus timing-dependent responses similar to those in DCN.…”

mentioning

confidence: 72%

“…A variety of learning rules reflecting STDP have been observed in the brain stem (Koehler and Shore 2013a;Tzounopoulos et al 2004) and cortex (Dahmen et al 2008;Egger et al 1999;Letzkus et al 2006;Schnupp et al 2006). Bimodal auditory-somatosensory plasticity in DCN modulates spontaneous and tone-evoked activity that is stimulus-timing dependent (Koehler and Shore 2013a).…”

Section: Discussionmentioning

confidence: 99%

“…Somatosensory convergence with auditory neurons as early in the pathway as the dorsal cochlear nucleus (DCN; Kanold and Young 2001;Shore 2005;Zhou et al 2007) is a potential etiology for tinnitus following noise exposure (Dehmel et al 2012b;Kaltenbach and McCaslin 1996;Koehler et al 2011;Koehler and Shore 2013b). Somatosensory-auditory bimodal stimulation results in long-lasting changes in neural firing rates in DCN (Dehmel et al 2012b) that are stimulus timing dependent (Koehler and Shore, 2013a), consistent with in vitro results showing spike timing-dependent plasticity (STDP) at parallel-fiber synapses (Tzounopoulos et al 2004). Furthermore, application of noise overexposure leading to tinnitus altered the stimulus timing-dependent rules from Hebbian to anti-Hebbian, with broader windows of enhancement than in sham-controls or noise-exposed animals without tinnitus (Koehler and Shore 2013b).…”

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confidence: 99%

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Bimodal stimulus timing-dependent plasticity in primary auditory cortex is altered after noise exposure with and without tinnitus

Basura

Koehler

Shore

2015

Journal of Neurophysiology

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Basura GJ, Koehler SD, Shore SE. Bimodal stimulus timingdependent plasticity in primary auditory cortex is altered after noise exposure with and without tinnitus. J Neurophysiol 114: 3064 -3075, 2015. First published August 19, 2015 doi:10.1152/jn.00319.2015.-Central auditory circuits are influenced by the somatosensory system, a relationship that may underlie tinnitus generation. In the guinea pig dorsal cochlear nucleus (DCN), pairing spinal trigeminal nucleus (Sp5) stimulation with tones at specific intervals and orders facilitated or suppressed subsequent tone-evoked neural responses, reflecting spike timing-dependent plasticity (STDP). Furthermore, after noiseinduced tinnitus, bimodal responses in DCN were shifted from Hebbian to anti-Hebbian timing rules with less discrete temporal windows, suggesting a role for bimodal plasticity in tinnitus. Here, we aimed to determine if multisensory STDP principles like those in DCN also exist in primary auditory cortex (A1), and whether they change following noise-induced tinnitus. Tone-evoked and spontaneous neural responses were recorded before and 15 min after bimodal stimulation in which the intervals and orders of auditory-somatosensory stimuli were randomized. Tone-evoked and spontaneous firing rates were influenced by the interval and order of the bimodal stimuli, and in sham-controls Hebbian-like timing rules predominated as was seen in DCN. In noise-exposed animals with and without tinnitus, timing rules shifted away from those found in sham-controls to more anti-Hebbian rules. Only those animals with evidence of tinnitus showed increased spontaneous firing rates, a purported neurophysiological correlate of tinnitus in A1. Together, these findings suggest that bimodal plasticity is also evident in A1 following noise damage and may have implications for tinnitus generation and therapeutic intervention across the central auditory circuit.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 57%

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confidence: 72%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Bimodal stimulus timing-dependent plasticity in primary auditory cortex is altered after noise exposure with and without tinnitus

Basura

Koehler

Shore

2015

Journal of Neurophysiology

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Reversing Synchronized Brain Circuits Using Targeted Auditory-Somatosensory Stimulation to Treat Phantom Percepts

et al. 2023

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ImportanceAnimal models have shown altered dorsal cochlear nucleus circuitry in animals that develop tinnitus; however, precise treatment using bisensory (auditory and somatosensory) stimuli can reverse altered neural patterns and lessen tinnitus.ObjectiveTo confirm and extend the findings of a pilot study, which suggested an increased efficacy of bisensory stimulation, to a clinical trial with a greater duration and greater number of participants.Design, Setting, and ParticipantsThis double-blind, crossover, single-center randomized clinical trial was conducted from March 2019, with a 3-month follow-up per participant ending in July 2022. Eligible adults were recruited from the University of Michigan Health System in Ann Arbor, Michigan. Eligibility criteria included bothersome tinnitus (Tinnitus Functional Index [TFI] score, ≥17 points), somatic tinnitus, normal to moderate hearing loss, and no other tinnitus treatments in the 6 months prior to the trial. Included participants were randomized to either treatment group 1, which received active (bisensory) treatment, or group 2, which received the control (auditory-only) treatment. Results were analyzed using intent-to-treat (ITT) and per protocol (PP) populations.InterventionPrecisely timed bisensory (combined auditory and somatosensory) treatment was delivered through a portable, custom, take-home device that was provided to each participant for daily, at-home treatments. Group 1 participants received 30 minutes per day of the bisensory treatment for 6 weeks, followed by a 6-week washout phase, and then 30 minutes per day of the auditory-only treatment followed by a second 6-week washout phase. Group 2 participants received the auditory-only treatment first, followed by a washout phase, and then the bisensory treatment followed by a second washout phase.Main Outcomes and MeasuresPrimary end points were changes in TFI score and tinnitus loudness level from baseline through week 6 and week 12.ResultsOf 337 screened individuals, 99 (mean [SD] age, 47 [12.7] years; 59 males [60%]; 85 with non-Hispanic White [86%] race and ethnicity) were enrolled into the study and randomized to treatment group 1 (n = 49) or group 2 (n = 50). The active but not the control treatment resulted in clinically significant decreases in TFI scores at week 6 of phase 1 (ITT population: –12.0 [95% CI, –16.9 to –7.9] points; P &lt; .001; PP population: –13.2 [95% CI, –16.0 to –10.5] points; P &lt; .001). Decreases in tinnitus loudness level were greater than 6 dB sensation level (SL; &gt;half as loud) at week 6 for the bisensory treatment group, with little effect for the auditory-only treatment control group at week 6 of phase 1 (ITT population: –5.8 [95% CI, –9.5 to –2.2] dB; P = .08; PP population: –7.2 [95% CI, –11.4 to –3.1] dB; P = .03), and up to 11 dB SL at week 12 of phase 2 (ITT population: –10.9 [95% CI, –15.2 to –6.5] dB; P = .001; PP population: –14.1 [95% CI, –18.4 to –9.8] dB; P &lt; .001). Decreased tinnitus loudness level and TFI scores extended into the washout phase, indicating a prolonged treatment effect.Conclusions and RelevanceThis trial found that precisely timed bisensory treatment using stimuli and timing developed in a validated animal model was effective for adults with somatic tinnitus. Prolonged reduction in tinnitus symptoms can result from using an extended treatment duration.Trial RegistrationClinicalTrials.gov Identifier: NCT03621735

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Bimodal Auditory Electrical Stimulation for the Treatment of Tinnitus: Preclinical and Clinical Studies

Riffle

Martel

Jones

et al. 2020

The Behavioral Neuroscience of Tinnitus

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Stimulus-Timing Dependent Multisensory Plasticity in the Guinea Pig Dorsal Cochlear Nucleus

Cited by 47 publications

References 53 publications

Bimodal stimulus timing-dependent plasticity in primary auditory cortex is altered after noise exposure with and without tinnitus

Bimodal stimulus timing-dependent plasticity in primary auditory cortex is altered after noise exposure with and without tinnitus

Reversing Synchronized Brain Circuits Using Targeted Auditory-Somatosensory Stimulation to Treat Phantom Percepts

Bimodal Auditory Electrical Stimulation for the Treatment of Tinnitus: Preclinical and Clinical Studies

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