Reorganization of auditory cortex after neonatal high frequency cochlear hearing loss

doi:10.1016/0378-5955(91)90131-R

Hearing Research

Volume 54, Issue 1, July 1991, Pages 11-19

https://doi.org/10.1016/0378-5955(91)90131-R Get rights and content

Abstract

Cochleotopic representation in cortex (AI) is extensively reorganized in cats having neonatal, bilateral high frequency cochlear hearing loss. Anterior areas of AI, normally devoted to high frequencies, contain neurons which are almost all tuned to one lower frequency. This frequency corresponds, at the level of the cochlea, to the border between normal and damaged haircell regions.

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Regulation of auditory plasticity during critical periods and following hearing loss
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Citation Excerpt :
Rodent studies indicate that complete sensorineural hearing loss during development disrupts synaptic inhibition and increases excitability throughout the central auditory pathway, resulting in broadened frequency tuning (reviewed in Sanes and Bao, 2009; Takesian et al., 2009). Neonatal high frequency hearing loss induced through cochlear lesions or traumatic noise exposure alters cortical tonotopy, shifting the tuning preference of neurons in high frequency regions to lower frequencies (Eggermont and Komiya, 2000; Harrison et al., 1991). Even transient hearing loss during development, such as that experienced by children with otitis media, can result in persistent changes in inhibitory synapses (Mowery et al., 2015, 2019; Takesian et al., 2012) that could contribute to sustained perceptual deficits later in life (Caras and Sanes, 2015; Takesian et al., 2012; Whitton and Polley, 2011).
Sensory input has profound effects on neuronal organization and sensory maps in the brain. The mechanisms regulating plasticity of the auditory pathway have been revealed by examining the consequences of altered auditory input during both developmental critical periods—when plasticity facilitates the optimization of neural circuits in concert with the external environment—and in adulthood—when hearing loss is linked to the generation of tinnitus. In this review, we summarize research identifying the molecular, cellular, and circuit-level mechanisms regulating neuronal organization and tonotopic map plasticity during developmental critical periods and in adulthood. These mechanisms are shared in both the juvenile and adult brain and along the length of the auditory pathway, where they serve to regulate disinhibitory networks, synaptic structure and function, as well as structural barriers to plasticity. Regulation of plasticity also involves both neuromodulatory circuits, which link plasticity with learning and attention, as well as ascending and descending auditory circuits, which link the auditory cortex and lower structures. Further work identifying the interplay of molecular and cellular mechanisms associating hearing loss-induced plasticity with tinnitus will continue to advance our understanding of this disorder and lead to new approaches to its treatment.
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Postnatal maturation of cortical circuits is marked by changes in connectivity, subunit composition of synaptic receptors, strength, as well as capacity for plasticity of excitatory and inhibitory synapses. Together, these factors shape the responsiveness of cortical neurons to sensory stimuli and contribute to establishing functional circuits. Experience plays a crucial role in the postnatal process of maturation, especially during windows of heightened plasticity known as sensitive periods. In this chapter, we bring together results from studies that examined the mechanisms underlying postnatal development of excitatory and inhibitory synapses and review them in context of studies investigating sensory circuit function. We report extant literature highlighting common mechanisms of maturation across visual, somatosensory, and auditory cortex, discuss similarities and differences in the time course of maturation and experience-dependent plasticity for all three cortices, and highlight emerging ideas about the contribution of excitation and inhibition in developing cortical circuits.
In vivo transcranial flavoprotein autofluorescence imaging of tonotopic map reorganization in the mouse auditory cortex with impaired auditory periphery
2019, Hearing Research
Citation Excerpt :
Thus, most plasticity in the AC involves changes in the balance between excitatory vs. inhibitory synapses within existing and newly formed patterns of connectivity (for review, Irvine, 2018). In the AC, researchers have reported tonotopic remapping following ototoxic insult in several animal species, including the cat (Harrison et al., 1991), guinea pig (Popelár et al., 1994), chinchilla (Kakigi et al., 2000; Qiu et al., 2000), ferret (Allman et al., 2009), and macaque monkey (Schwaber et al., 1993). For example, Kakigi et al. (2000) reported that, in the A1 of adult chinchillas exposed to amikacin-induced basal cochlear hair cell lesions, there is a rearrangement of cortical responses that leads to a preference for low characteristic frequency responses at regions of the cortex that are normally responsive to higher frequency stimuli at threshold.
Ototoxic-drug-induced hearing disturbances in the auditory periphery are associated with tonotopic map reorganization and neural activity modulation, as well as changes in neural correlates in the central auditory pathway, including the auditory cortex (AC). Previous studies have reported that peripheral auditory impairment induces AC plasticity that involves changes in the balance of excitatory vs. inhibitory synapses, within existing and newly forming patterns of connectivity. Although we know that such plastic changes modulate sound-evoked neural responses and the organization of tonotopic maps in the primary AC (A1), little is known about the effects of peripheral impairment on other frequency-organized AC subfields, such as the anterior auditory field (AAF) and the secondary auditory cortex (A2). Therefore, to examine ototoxic-drug-induced spatiotemporal effects on AC subfields, we measured sound-evoked neural activity in mice before and after the administration of kanamycin sulfate (1 mg/g body weight) and bumetanide (0.05 mg/g body weight), using in vivo transcranial flavoprotein autofluorescence imaging over a 4-week period. At first, ototoxic treatment gradually reduced responses driven by tone bursts with lower- (≤8 kHz) and middle- (e.g., 16 kHz) range frequencies in all AC subfields. Subsequently, response intensities in the A1 recovered to more than 78% of the pre-drug condition; however, in the AAF and A2, they remained significantly lower and were unchanged over 3 weeks. Furthermore, after drug administration, the best frequency (BF) areas of the lower (4 and 8 kHz) and higher (25 and 32 kHz) ranges in all subfields were reduced and shifted to those of a middle range (centered around 16 kHz) during the 3 weeks following drug administration. Our results also indicated that, compared with A1, BF distributions in the AAF and A2 were sharper around 16 kHz 3 weeks after drug administration. These results indicate that the ototoxic-damage-induced tonotopic map reorganizations that occurred in each of the three AC subfields were similar, but that there were subfield-dependent differences in the extent of response intensities and in the activated areas that were responsive to tone bursts with specific frequencies. Thus, by examining cortical reorganization induced by ototoxic drugs, we may contribute to the understanding of how this reorganization can be caused by peripheral damage.
Plasticity in the auditory system
2018, Hearing Research
Over the last 30 years a wide range of manipulations of auditory input and experience have been shown to result in plasticity in auditory cortical and subcortical structures. The time course of plasticity ranges from very rapid stimulus-specific adaptation to longer-term changes associated with, for example, partial hearing loss or perceptual learning. Evidence for plasticity as a consequence of these and a range of other manipulations of auditory input and/or its significance is reviewed, with an emphasis on plasticity in adults and in the auditory cortex. The nature of the changes in auditory cortex associated with attention, memory and perceptual learning depend critically on task structure, reward contingencies, and learning strategy. Most forms of auditory system plasticity are adaptive, in that they serve to optimize auditory performance, prompting attempts to harness this plasticity for therapeutic purposes. However, plasticity associated with cochlear trauma and partial hearing loss appears to be maladaptive, and has been linked to tinnitus. Three important forms of human learning-related auditory system plasticity are those associated with language development, musical training, and improvement in performance with a cochlear implant. Almost all forms of plasticity involve changes in synaptic excitatory – inhibitory balance within existing patterns of connectivity. An attractive model applicable to a number of forms of learning-related plasticity is dynamic multiplexing by individual neurons, such that learning involving a particular stimulus attribute reflects a particular subset of the diverse inputs to a given neuron being gated by top-down influences. The plasticity evidence indicates that auditory cortex is a component of complex distributed networks that integrate the representation of auditory stimuli with attention, decision and reward processes.
Disappearance of contralateral dominant neural activity of auditory cortex after single-sided deafness in adult rats
2017, Neuroscience Letters
Citation Excerpt :
In the serial analysis of peak amplitude, the sum of the spikes and peak amplitude revealed short-term changes (4 weeks) and gradual adaptation in both hemispheres. These data suggest that plastic changes in the brain are not limited to neonatal animals as previously reported [11,12,29] but also occur in adult animals [3,26]. In addition, these data confirmed the contralateral dominance of the auditory pathway and also revealed its absence after SSD.
Hearing loss in mature ears can cause functional reorganization of the auditory cortex. The functional reorganization is speculated to negatively affect the outcome of hearing rehabilitation. Therefore, once hearing loss occurs, it is important to provide auditory input before extensive reorganization in the auditory pathways. We investigated the neural plasticity in auditory cortex after single-sided deafness (SSD) in an adult rat model. The animals were divided into two groups: a normal hearing (NH) and the SSD group. The neural recordings of the SSD group were conducted at different time points (2, 4, 6 and 8 weeks) after cochlear ablation. The multi-unit activity was discriminated on the sum of spikes, peak amplitude, onset latency, peak latency, and responsive area based on the peak amplitude. The auditory cortical reorganization was observed after SSD. The contralateral dominance of peak amplitude and latency that normally occur in NH group were not present in the SSD group, replaced by higher amplitude and faster response in ipsilateral cortex. According to serial recordings at different time points after SSD, different phases in the response of the auditory cortex were speculated. Compared with normal hearing, alteration of contralateral dominance was observed because of the functional reorganization of the auditory cortex after SSD.
Acquired hearing loss and brain plasticity
2017, Hearing Research
Acquired hearing loss results in an imbalance of the cochlear output across frequency. Central auditory system homeostatic processes responding to this result in frequency specific gain changes consequent to the emerging imbalance between excitation and inhibition. Several consequences thereof are increased spontaneous firing rates, increased neural synchrony, and (in adults) potentially restricted to the auditory thalamus and cortex a reorganization of tonotopic areas. It does not seem to matter much whether the hearing loss is acquired neonatally or in adulthood. In humans, no clear evidence of tonotopic map changes with hearing loss has so far been provided, but frequency specific gain changes are well documented. Unilateral hearing loss in addition makes brain activity across hemispheres more symmetrical and more synchronous. Molecular studies indicate that in the brainstem, after 2–5 days post trauma, the glutamatergic activity is reduced, whereas glycinergic and GABAergic activity is largely unchanged. At 2 months post trauma, excitatory activity remains decreased but the inhibitory one is significantly increased. In contrast protein assays related to inhibitory transmission are all decreased or unchanged in the brainstem, midbrain and auditory cortex. Comparison of neurophysiological data with the molecular findings during a time-line of changes following noise trauma suggests that increases in spontaneous firing rates are related to decreases in inhibition, and not to increases in excitation. Because noise-induced hearing loss in cats resulted in a loss of cortical temporal processing capabilities, this may also underlie speech understanding in humans.

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Reorganization of auditory cortex after neonatal high frequency cochlear hearing loss

Abstract

Properties of auditory nerve responses in the absence of outer haircells

J. Neurophysiol.

The sharpening of cochlear frequency selectivity in the normal and abnormal cochlea

Audiology

Rate-versus-intensity functions and related AP responses in normal and pathological guinea pig and human cochleas

J. Acoust. Soc. Am.

Cochlear fibre responses in guinea pigs with well defined cochlear lesions

Scand. Audiol. Suppl.

Single cochlear fiber responses in guinea pigs with long-term endolymphatic hydrops

Hear. Res.

Binocular interaction in striate cortex of kittens reared with artificial squint

J. Neurophysiol.

Binaural columns in the primary field (AI) of cat auditory cortex

Brain Res.

The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals

Reorganization of retinotopic cortical maps in adult mammals after lesion of the retina

Science

Auditory nerve activity in cats with normal and abnormal cochleas

Auditory nerve activity in cats exposed to ototoxic drugs and high intensity sounds

Ann. Otol. Rhinol. Laryngol.

Acute and chronic effects of acoustic trauma. Cochlear pathology and auditory nerve pathophysiology