Developmental Hearing Loss Disrupts Synaptic Inhibition: Implications for Auditory Processing

Takesian, Anne E.; Kotak, Vibhakar C.; Sanes, Dan H.

doi:10.2217/fnl.09.5

Cited by 67 publications

(57 citation statements)

References 217 publications

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“…This discrepancy between the current results and results summarized in Takesian et al, 2009 may suggest that effect of developmental PCB exposure causes separate, direct effects on the AC. An alternative explanation is that the mechanisms for disrupting peripheral hearing structures after developmental PCB exposure differ from those seen when peripheral hearing structures are physically damaged, such as methods described in Takesian et al (2009) for inducing conductive hearing loss.…”

Section: Discussioncontrasting

confidence: 99%

“…It is possible that PCBs are acting indirectly, given that peripheral hearing loss during a critical period of development is associated with changes in inhibitory postsynaptic currents, electrophysiological measures, and long-term plasticity in the AC of adult animals (Mowery et al, 2015; Kotak et al, 2007). However, in previous work, peripheral hearing loss is associated with a decrease in synaptic inhibition (Takesian et al, 2009), while the current study suggests that there may be an upregulation of GABAergic transmission in the AC. This discrepancy between the current results and results summarized in Takesian et al, 2009 may suggest that effect of developmental PCB exposure causes separate, direct effects on the AC.…”

Section: Discussioncontrasting

confidence: 70%

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Developmental exposure to PCBs alters the activation of the auditory cortex in response to GABA A antagonism

et al. 2016

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Developmental exposure of rats to polychlorinated biphenyls (PCBs) causes impairments in hearing and in the functioning of peripheral and central auditory structures. Additionally, recent work from our laboratory has demonstrated an increase in audiogenic seizures. The current study aimed to further characterize the effects of PCBs on auditory brain structures by investigating whether developmental exposure altered the magnitude of activation in the auditory cortex (AC) in response to electrical stimulation of thalamocortical afferents. Long-Evans female rats were fed cookies containing either 0 or 6 mg/kg of an environmental PCB mixture daily from 4 weeks prior to breeding until postnatal day 21. Brain slices containing projections from the thalamus to the AC were collected from adult female offspring and were bathed in artificial cerebrospinal fluid (aCSF) alone, aCSF containing a gamma-aminobutyric acid (GABA) receptor antagonist (200 nM SR95531), and aCSF containing an and N-methyl-D-aspartate (NMDA) receptor antagonist (50μM AP5). During each of these drug conditions, electrical stimulations ranging from 25-600 μA were delivered to the thalamocortical afferents. Activation of the AC was measured using flavoprotein autofluorescence imaging. Although there were no differences seen between treatment groups in the aCSF condition, there were significant increases in the ratio of aCSF/SR95531 activation in slices from PCB-exposed animals compared to control animals. This effect was seen in both the upper and lower layers of the AC. No differences in activation were noted between treatment groups when slices were exposed to AP5. These data suggest that developmental PCB exposure leads to increased sensitivity to antagonism of GABAA receptors in the AC without a change in NMDA-mediated intrinsic excitability.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussioncontrasting

confidence: 70%

Developmental exposure to PCBs alters the activation of the auditory cortex in response to GABA A antagonism

et al. 2016

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“…This demonstrates a fairly brief critical period for use-dependent strengthening of synaptic connections. A larger set of studies has reported that a period of developmental deprivation (i.e., hearing loss) can lead to profound changes in synaptic strength along the entire auditory CNS (Takesian et al, 2009). Figure 10B shows one set of examples from the gerbil auditory cortex following about 1 week of hearing loss (Takesian et al, 2010).…”

Section: Synaptic Correlates Of Central Auditory Development and Plastimentioning

confidence: 99%

A Behavioral Framework to Guide Research on Central Auditory Development and Plasticity

Sanes

Woolley

2011

Neuron

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The auditory CNS is influenced profoundly by sounds heard during development. Auditory deprivation and augmented sound exposure can each perturb the maturation of neural computations as well as their underlying synaptic properties. However, we have learned little about the emergence of perceptual skills in these same model systems, and especially how perception is influenced by early acoustic experience. Here, we argue that developmental studies must take greater advantage of behavioral benchmarks. We discuss quantitative measures of perceptual development, and suggest how they can play a much larger role in guiding experimental design. Most importantly, including behavioral measures will allow us to establish empirical connections among environment, neural development, and perception.

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“…Investigators have found strong evidence to suggest that peripheral damage leads to a down-regulation of inhibitory synapses, stemming from a decrease in statistically meaningful sensory inputs from the environment (Robertson and Irvine, 1989; Kotak et al, 2005; Takesian et al, 2009, 2013). This process, termed “negative plasticity,” serves to re-establish homeostasis in the auditory cortex, and may explain many of the features associated with altered processing accompanying damage to the auditory system (Syka, 2002; Takesian et al, 2009, 2011).…”

Section: Introductionmentioning

confidence: 99%

Shaping the aging brain: role of auditory input patterns in the emergence of auditory cortical impairments

Kamal¹,

Holman²,

Villers-Sidani³

2013

Front. Syst. Neurosci.

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Age-related impairments in the primary auditory cortex (A1) include poor tuning selectivity, neural desynchronization, and degraded responses to low-probability sounds. These changes have been largely attributed to reduced inhibition in the aged brain, and are thought to contribute to substantial hearing impairment in both humans and animals. Since many of these changes can be partially reversed with auditory training, it has been speculated that they might not be purely degenerative, but might rather represent negative plastic adjustments to noisy or distorted auditory signals reaching the brain. To test this hypothesis, we examined the impact of exposing young adult rats to 8 weeks of low-grade broadband noise on several aspects of A1 function and structure. We then characterized the same A1 elements in aging rats for comparison. We found that the impact of noise exposure on A1 tuning selectivity, temporal processing of auditory signal and responses to oddball tones was almost indistinguishable from the effect of natural aging. Moreover, noise exposure resulted in a reduction in the population of parvalbumin inhibitory interneurons and cortical myelin as previously documented in the aged group. Most of these changes reversed after returning the rats to a quiet environment. These results support the hypothesis that age-related changes in A1 have a strong activity-dependent component and indicate that the presence or absence of clear auditory input patterns might be a key factor in sustaining adult A1 function.

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Developmental Hearing Loss Disrupts Synaptic Inhibition: Implications for Auditory Processing

Cited by 67 publications

References 217 publications

Developmental exposure to PCBs alters the activation of the auditory cortex in response to GABA A antagonism

Developmental exposure to PCBs alters the activation of the auditory cortex in response to GABA A antagonism

A Behavioral Framework to Guide Research on Central Auditory Development and Plasticity

Shaping the aging brain: role of auditory input patterns in the emergence of auditory cortical impairments

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