Hearing Loss Alters Serotonergic Modulation of Intrinsic Excitability in Auditory Cortex

Rao, Deepti; Basura, Gregory J.; Roche, Joseph P.; Daniels, Scott David; Mancilla, Jaime G.; Manis, Paul B.

doi:10.1152/jn.01092.2009

Cited by 27 publications

(21 citation statements)

References 62 publications

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“…Adaptation to the pronounced differences between the neural activation evoked by electrical stimulation and by physiological firing of inner hair cells consists of other significant processes that may take place during this period . Deafness is known to cause increased spontaneous activity, tonotopic distortion, homeostatic changes, and strengthening of non-auditory inputs in auditory cortex (Kral 2007;Rao et al 2010). It is likely that the time a cochlear implant recipient spends adapting to the device is a period of recovery from sensory deprivation rather than a protracted period required for learning to compensate for degraded speech.…”

Section: Discussionmentioning

confidence: 99%

Neural Mechanisms Supporting Robust Discrimination of Spectrally and Temporally Degraded Speech

Ranasinghe

Vrana

Matney

et al. 2012

JARO

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Cochlear implants provide good speech discrimination ability despite highly limited amount of information they transmit compared with normal cochlea. Noise vocoded speech, simulating cochlear implants in normal hearing listeners, have demonstrated that spectrally and temporally degraded speech contains sufficient cues to provide accurate speech discrimination. We hypothesized that neural activity patterns generated in the primary auditory cortex by spectrally and temporally degraded speech sounds will account for the robust behavioral discrimination of speech. We examined the behavioral discrimination of noise vocoded consonants and vowels by rats and recorded neural activity patterns from rat primary auditory cortex (A1) for the same sounds. We report the first evidence of behavioral discrimination of degraded speech sounds by an animal model. Our results show that rats are able to accurately discriminate both consonant and vowel sounds even after significant spectral and temporal degradation. The degree of degradation that rats can tolerate is comparable to human listeners. We observed that neural discrimination based on spatiotemporal patterns (spike timing) of A1 neurons is highly correlated with behavioral discrimination of consonants and that neural discrimination based on spatial activity patterns (spike count) of A1 neurons is highly correlated with behavioral discrimination of vowels. The results of the current study indicate that speech discrimination is resistant to degradation as long as the degraded sounds generate distinct patterns of neural activity.

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Section: Discussionmentioning

confidence: 99%

Neural Mechanisms Supporting Robust Discrimination of Spectrally and Temporally Degraded Speech

Ranasinghe

Vrana

Matney

et al. 2012

JARO

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“…In the gerbil LSO and the IC of mouse and Mexican free-tailed bat, agonists that activate this receptor type depress responsiveness to the electrical stimulation of input fibers or to auditory stimuli (Fitzgerald and Sanes, 1999; Hurley, 2006, 2007). There is also evidence for a post-synaptic site of serotonin-evoked suppression in the cortical slice preparation; application of serotonin decreases the spiking response and adaptation to injected current, and lowers the input resistance (Rao et al, 2010). Other mechanisms for suppression may be presynaptic.…”

Section: Physiological Effects Of Serotoninmentioning

confidence: 99%

Context-dependent modulation of auditory processing by serotonin

Hurley

Hall

2011

Hearing Research

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Context-dependent plasticity in auditory processing is achieved in part by physiological mechanisms that link behavioral state to neural responses to sound. The neuromodulator serotonin has many characteristics suitable for such a role. Serotonergic neurons are extrinsic to the auditory system but send projections to most auditory regions. These projections release serotonin during particular behavioral contexts. Heightened levels of behavioral arousal and specific extrinsic events, including stressful or social events, increase serotonin availability in the auditory system. Although the release of serotonin is likely to be relatively diffuse, highly specific effects of serotonin on auditory neural circuitry are achieved through the localization of serotonergic projections, and through a large array of receptor types that are expressed by specific subsets of auditory neurons. Through this array, serotonin enacts plasticity in auditory processing in multiple ways. Serotonin changes the responses of auditory neurons to input through the alteration of intrinsic and synaptic properties, and alters both short- and long-term forms of plasticity. The infrastructure of the serotonergic system itself is also plastic, responding to age and cochlear trauma. These diverse findings support a view of serotonin as a widespread mechanism for behaviorally relevant plasticity in the regulation of auditory processing. This view also accommodates models of how the same regulatory mechanism can have pathological consequences for auditory processing.

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“…This was true even though other receptor genes did not show these effects. Rao et al (2010) found similarly dramatic effects of sham surgical procedures in the auditory cortex. In their study, real and sham cochleotomies had similar effects on the ability of serotonin to decrease firing rates, input resistance, and spike rate adaptation.…”

Section: Discussionmentioning

confidence: 85%

“…Damage to the auditory system by trauma, aging, or peripheral deprivation can cause a myriad of molecular and physiological changes (Argence et al, 2006; Dong et al, 2010a,b; Holt et al, 2005; Manzoor et al, 2013; Mossop et al, 2000; Rao et al, 2010; Tadros et al, 2007; Vale and Sanes, 2002). These changes may be viewed as compensatory or even pathological, and could contribute to aberrant perceptual states such as tinnitus (Eggermont and Roberts, 2004; Knipper et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…The density of neuromodulatory fibers, the profiles of axonal contacts, and the expression of particular receptor types are altered by damage to sensory organs (Holt et al, 2005; Kang et al, 2013; Qu et al, 2000; Rao et al, 2010; Rhoades et al, 1990; Tadros et al, 2007; Vizuete et al, 1993). One such neuromodulatory pathway is the serotonergic system.…”

Section: Introductionmentioning

confidence: 99%

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Acoustic trauma triggers upregulation of serotonin receptor genes

Smith¹,

Kwon²,

Navarro³

et al. 2014

Hearing Research

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Hearing loss induces plasticity in excitatory and inhibitory neurotransmitter systems in auditory brain regions. Excitatory-inhibitory balance is also influenced by a range of neuromodulatory regulatory systems, but less is known about the effects of auditory damage on these networks. In this work, we studied the effects of acoustic trauma on neuromodulatory plasticity in the auditory midbrain of CBA/J mice. Quantitative PCR was used to measure the expression of serotonergic and GABAergic receptor genes in the inferior colliculus (IC) of mice that were unmanipulated, sham controls with no hearing loss, and experimental individuals with hearing loss induced by exposure to a 116 dB, 10 kHz pure tone for 3 hours. Acoustic trauma induced substantial hearing loss that was accompanied by selective upregulation of two serotonin receptor genes in the IC. The Htr1B receptor gene was upregulated tenfold following trauma relative to shams, while the Htr1A gene was upregulated threefold. In contrast, no plasticity in serotonin receptor gene expression was found in the hippocampus, a region also innervated by serotonergic projections. Analyses in the IC demonstrated that acoustic trauma also changed the coexpression of genes in relation to each other, leading to an overexpression of Htr1B compared to other genes.. These data suggest that acoustic trauma induces serotonergic plasticity in the auditory system, and that this plasticity may involve comodulation of functionally-linked receptor genes.

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Hearing Loss Alters Serotonergic Modulation of Intrinsic Excitability in Auditory Cortex

Cited by 27 publications

References 62 publications

Neural Mechanisms Supporting Robust Discrimination of Spectrally and Temporally Degraded Speech

Neural Mechanisms Supporting Robust Discrimination of Spectrally and Temporally Degraded Speech

Context-dependent modulation of auditory processing by serotonin

Acoustic trauma triggers upregulation of serotonin receptor genes

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