Homeostatic plasticity drives tinnitus perception in an animal model

Yang, Sungchil; Weiner, Benjamin; Zhang, Li S.; Cho, Sung‐Jin; Bao, Shaowen

doi:10.1073/pnas.1107998108

Cited by 249 publications

(257 citation statements)

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“…Following hearing loss, cortical response thresholds are higher at the affected frequencies and a subsequent loss of inhibition follows (25). This weakened inhibition has been linked with the perception of tinnitus (29). Tinnitus may develop as excitation and inhibition find a new balance following the reduction of inhibition.…”

Section: Discussionmentioning

confidence: 99%

“…Reduction of inhibition is a component of many neurological conditions, including hearing loss, aging, TBI, and neuropsychiatric diseases (19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29). Following hearing loss, cortical response thresholds are higher at the affected frequencies and a subsequent loss of inhibition follows (25).…”

Section: Discussionmentioning

confidence: 99%

“…Loss of inhibitory interneurons is observed in conditions that affect cortical processing in humans, and in animal models of human disorders, including aging (18,19), autism (20), schizophrenia (21)(22)(23), traumatic brain injury (TBI) (24), hearing loss (25)(26)(27)(28), and tinnitus (29). Often, a particular disease is associated with a specific deficit in a subset of interneurons.…”

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confidence: 99%

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Chronic reduction in inhibition reduces receptive field size in mouse auditory cortex

Seybold

Stanco

Cho³

et al. 2012

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

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Inhibitory interneurons regulate the responses of cortical circuits. In auditory cortical areas, inhibition from these neurons narrows spectral tuning and shapes response dynamics. Acute disruptions of inhibition expand spectral receptive fields. However, the effects of long-term perturbations of inhibitory circuitry on auditory cortical responses are unknown. We ablated ∼30% of dendrite-targeting cortical inhibitory interneurons after the critical period by studying mice with a conditional deletion of Dlx1. Following the loss of interneurons, baseline firing rates rose and tone-evoked responses became less sparse in auditory cortex. However, contrary to acute blockades of inhibition, the sizes of spectral receptive fields were reduced, demonstrating both higher thresholds and narrower bandwidths. Furthermore, long-latency responses at the edge of the receptive field were absent. On the basis of changes in response dynamics, the mechanism for the reduction in receptive field size appears to be a compensatory loss of corticocortically (CC) driven responses. Our findings suggest chronic conditions that feature changes in inhibitory circuitry are not likely to be well modeled by acute network manipulations, and compensation may be a critical component of chronic neuronal conditions. P rocessing of auditory information in the auditory cortex underlies the conscious perception of sound and speech comprehension. Inhibitory interneurons, representing ∼20% of cortical neurons (1), regulate this processing by shaping the spectral tuning (2-13), temporal tuning (14-16), and response dynamics of local excitatory neurons (5-11). Inhibitory interneurons form multiple subtypes on the basis of morphology, physiology, and biochemistry (1, 17) that likely serve distinct roles in cortical processing.Loss of inhibitory interneurons is observed in conditions that affect cortical processing in humans, and in animal models of human disorders, including aging (18, 19), autism (20), schizophrenia (21-23), traumatic brain injury (TBI) (24), hearing loss (25-28), and tinnitus (29). Often, a particular disease is associated with a specific deficit in a subset of interneurons. For example, rodent models of autism demonstrate a loss of parvalbumin positive (PV + ) interneurons (20), whereas aging and TBI models show a greater loss of somatostatin (SST) + interneurons than other interneuron populations (19,24). The disruption of specific interneuron populations may underlie the particular cognitive defects associated with each condition. Therefore, it is necessary to understand the effects following chronic reductions of particular interneuron subtypes.One mouse model of an adult-onset loss of dendrite-targeting interneurons (DTIs) is the Dlx1 mutant (30). Dlx1 encodes a homeobox transcription factor from the Dlx family that regulates the development, migration, and survival of cortical interneurons (30-32). In Dlx1 mutants, the other Dlx family members compensate for the deficiency and thereby allow interneurons to migrate into cortex (30)....

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Chronic reduction in inhibition reduces receptive field size in mouse auditory cortex

Seybold

Stanco

Cho³

et al. 2012

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

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“…However, selective hearing loss of high-frequency sound also increases neuronal responsiveness in the lesion projection zone (area representing high-frequency sound) through a selective repression of synaptic inhibition within the zone. This occurs despite the presence of normal input to the neighbouring cortical area representing lower-frequency sounds, indicating that homeostatic plasticity can occur in the presence of activity competition [60].…”

Section: Circuit Mechanisms: Competition Model and Beyondmentioning

confidence: 99%

A metaplasticity view of the interaction between homeostatic and Hebbian plasticity

Yee¹,

Hsu²,

Chen³

2017

Phil. Trans. R. Soc. B

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One contribution of 16 to a discussion meeting issue 'Integrating Hebbian and homeostatic plasticity'. Hebbian and homeostatic plasticity are two major forms of plasticity in the nervous system: Hebbian plasticity provides a synaptic basis for associative learning, whereas homeostatic plasticity serves to stabilize network activity. While achieving seemingly very different goals, these two types of plasticity interact functionally through overlapping elements in their respective mechanisms. Here, we review studies conducted in the mammalian central nervous system, summarize known circuit and molecular mechanisms of homeostatic plasticity, and compare these mechanisms with those that mediate Hebbian plasticity. We end with a discussion of 'local' homeostatic plasticity and the potential role of local homeostatic plasticity as a form of metaplasticity that modulates a neuron's future capacity for Hebbian plasticity.This article is part of the themed issue 'Integrating Hebbian and homeostatic plasticity'.

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“…However, this generally did not lead to cessation of the phantom phenomena (8), which underlines the crucial importance of the central nervous system for the pathophysiology of chronic tinnitus (8). We now know that tinnitus involves augmented stimulation all the way along the central auditory pathway which-similarly to phantom pain-arises as a compensatory reaction to the partial hearing loss experienced in most cases (9)(10)(11). Abnormal activity in somatosensory afferent nerves can also lead to increased activity in the central auditory pathway (e2-e4).…”

Section: Pathophysiologymentioning

confidence: 99%