Developmental hearing loss eliminates long-term potentiation in the auditory cortex

Abstract

Severe hearing loss during early development is associated with deficits in speech and language acquisition. Although functional studies have shown a deafness-induced alteration of synaptic strength, it is not known whether long-term synaptic plasticity depends on auditory experience. In this study, sensorineural hearing loss (SNHL) was induced surgically in developing gerbils at postnatal day 10, and excitatory synaptic plasticity was examined subsequently in a brain slice preparation that preserves the thalamorecipient auditory cortex. Extracellular stimuli were applied at layer 6 (L6), whereas evoked excitatory synaptic potentials (EPSPs) were recorded from L5 neurons by using a whole-cell current clamp configuration. In control neurons, the conditioning stimulation of L6 significantly altered EPSP amplitude for at least 1 h. Approximately half of neurons displayed long-term potentiation (LTP), whereas the other half displayed long-term depression (LTD). In contrast, SNHL neurons displayed only LTD after the conditioning stimulation of L6. Finally, the vast majority of neurons recorded from control prehearing animals (postnatal days 9 -11) displayed LTD after L6 stimulation. Thus, normal auditory experience may be essential for the maturation of synaptic plasticity mechanisms.deafness ͉ long-term depression S evere hearing loss is known to affect auditory processing in humans. This loss includes impairments of signal detection in noise or in a multiple source environment, and disruption of intensity discrimination, frequency discrimination, and temporal resolution (1-4). Even transient bouts of conductive hearing loss can disrupt auditory processing, and months or years may be required for normal perception to resolve (5, 6). Because severe hearing loss during development is implicated in the deficient acquisition of auditory perceptual skills and language, which presumably require learning, we have examined whether synaptic plasticity is also affected.At a structural level, hearing impairments can lead to neuron death or atrophy and alter process outgrowth (7). Furthermore, direct examination of neuron function in brain slice preparations from deaf animals has revealed significant physiological changes to intrinsic and synaptic properties. In both the inferior colliculus and auditory cortex (ACx), early sensorineural hearing loss (SNHL) alters the balance of excitatory and inhibitory synaptic strength (8-10). A similar disruption in synaptic physiology and certain intrinsic properties also occurs in the auditory brainstem of the congenitally deaf mutant mouse (11,12).Both long-term potentiation (LTP) and depression (LTD) have been characterized in a series of studies on the rat ACx (13-18). For example, an NMDA receptor-mediated LTP in the ACx can be induced by stimulation of afferents innervating the ACx via the white matter (13), whereas thalamo-and corticocortical synapse activation can induce LTD (16). These cellular mechanisms may serve as a substrate for use-dependent alteration of coding properties in...

Long-term, partially-reversible reorganization of frequency tuning in mature cat primary auditory cortex can be induced by passive exposure to moderate-level sounds

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Anatomical connections suitable for the direct processing of neuronal information of different modalities via the rodent primary auditory cortex

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A method to induce human cortical long-term potentiation by acoustic stimulation

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