Silvia Heid

Delayed Maturation and Sensitive Periods in the Auditory Cortex

Behavioral data indicate the existence of sensitive periods in the development of audition and language. Neurophysiological data demonstrate deficits in the cerebral cortex of auditory-deprived animals, mainly in reduced cochleotopy and deficits in corticocortical and corticothalamic loops. In addition to current spread in the cochlea, reduced cochleotopy leads to channel interactions after cochlear implantation. Deficits in corticocortical and corticothalamic loops interfere with normal processing of auditory activity in cortical areas. Thus, the deprived auditory cortex cannot mature normally in congenital deafness. This maturation can be achieved using auditory experience through cochlear implants. However, implantation is necessary within the sensitive period of the auditory system. The functional role of long-term potentiation and long-term depression, inhibition, cholinergic modulation and neurotrophins in auditory development and sensitive periods are discussed.

Cochlear implants: cortical plasticity in congenital deprivation.

Congenital auditory deprivation (deafness) leads to a dysfunctional intrinsic cortical microcircuitry. This chapter reviews these deficits with a particular emphasis on layer-specific activity within the primary auditory cortex. Evidence for a delay in activation of supragranular layers and reduction in activity in infragranular layers is discussed. Such deficits indicate the incompetence of the primary auditory cortex to not only properly process thalamic input and generate output within the infragranular layers, but also incorporate top-down modulations from higher order auditory cortex into the processing within primary auditory cortex. Such deficits are the consequence of a misguided postnatal development. Maturation of primary auditory cortex in deaf animals shows evidence of a developmental delay and further alterations in gross synaptic currents, spread of activation, and morphology of local field potentials recorded at the cortical surface. Additionally, degenerative changes can be observed. When hearing is initiated early in life (e.g., by chronic cochlear-implant stimulation), many of these deficits are counterbalanced. However, plasticity of the auditory cortex decreases with increasing age, so that a sensitive period for plastic adaptation can be demonstrated within the second to sixth months of life in the deaf cat. Potential molecular mechanisms of the existence of sensitive period are discussed. Data from animal research may be compared to electroencephalographic data obtained from cochlear-implanted congenitally deaf children. After cochlear implantation in humans, three phases of plastic adaptation can be observed: a fast one, taking place within the first few weeks after implantation, showing no sensitive period; a slower one, taking place within the first months after implantation (a sensitive period up to 4 years of age); and possibly a third, and the longest one, related to increasing activation of higher order cortical areas.

Response of the primary auditory cortex to electrical stimulation of the auditory nerve in the congenitally deaf white cat

Neural activity plays an important role in the development and maintenance of sensory pathways. However, while there is considerable experience using cochlear implants in both congenitally deaf adults and children, little is known of the effects of a hearing loss on the development of the auditory cortex. In the present study, cortical evoked potentials, field potentials, and multi- and single-unit activity evoked by electrical stimulation of the auditory nerve were used to study the functional organisation of the auditory cortex in the adult congenitally deaf white cat. The absence of click-evoked auditory brainstem responses during the first weeks of life demonstrated that these animals had no auditory experience. Under barbiturate anaesthesia, cortical potentials could be recorded from the contralateral auditory cortex in response to bipolar electrical stimulation of the cochlea in spite of total auditory deprivation. Threshold, morphology and latency of the evoked potentials varied with the location of the recording electrode, with response latency varying from 10 to 20 ms. There was evidence of threshold shifts with site of the cochlear stimulation in accordance with the known cochleotopic organisation of AI. Thresholds also varied with the configuration of the stimulating electrodes in accordance with changes previously observed in normal hearing animals. Single-unit recordings exhibited properties similar to the evoked potentials. Increasing stimulus intensity resulted in an increase in spike rate and a decrease in latency to a minimum of approximately 8 ms, consistent with latencies recorded in AI of previously normal animals (Raggio and Schreiner, 1994). Single-unit thresholds also varied with the configuration of the stimulating electrodes. Strongly driven responses were followed by a suppression of spontaneous activity. Even at saturation intensities the degree of synchronisation was less than observed when recording from auditory brainstem nuclei. Taken together, in these auditory deprived animals basic response properties of the auditory cortex of the congenitally deaf white cat appear similar to those reported in normal hearing animals in response to electrical stimulation of the auditory nerve. In addition, it seems that the auditory cortex retains at least some rudimentary level of cochleotopic organisation.

A model for prelingual deafness, the congenitally deaf white cat – population statistics and degenerative changes

Cochlear implantation in congenitally deaf children leads to electrical stimulation of an entirely naive central auditory system. In this case, processes of central auditory maturation are induced by the electric stimuli. For the study of these processes the deaf white cat (DWC) appears to be an appropriate model. However, a knowledge of the basic data of these animals is necessary before such a model may be used. This paper presents these data and is one of a series of publications concerning congenital deafness in children and cochlear implantation. In our strain 72% of the animals are totally deaf as judged by the absence of any brain stem evoked potentials at click intensities up to 120 dB SPL peak equivalent. Primarily, there is a degeneration of the entire organ of Corti during the first postnatal weeks. An absence of acoustically evoked brain stem responses in the early postnatal weeks shows that DWCs probably never have any hearing experience. Months after the degeneration of the organ of Corti, the spiral ganglion starts to degenerate from the midportion of the cochlea. However, even in adult cats (2 years), a sufficient number of functionally intact auditory afferents remain, which are suitable for electrical cochlear stimulation.

Erratum to “Development of Brainstem-Evoked Responses in Congenital Auditory Deprivation”

The caption of Figure 1 in the paper at doi:10.1155/2012/182767 has to be corrected as shown here. Also, should be corrected as follows: J. Tillein, S. Heid, E. Lang, R. Hartmann, and A. kral, “Development of brainstem-evoked responses in congenital auditory deprivation,” Neural Plasticity, vol. 2012, Article ID 182767, 11 Pages, 2012. s.a. urn:nbn:de:hebis:30:3-267673

Spatiotemporal Patterns of Cortical Activity with Bilateral Cochlear Implants in Congenital Deafness

Congenital deafness affects developmental processes in the auditory cortex. In this study, local field potentials (LFPs) were mapped at the cortical surface with microelectrodes in response to cochlear implant stimulation. LFPs were compared between hearing controls and congenitally deaf cats (CDCs). Pulsatile electrical stimulation initially evoked cortical activity in the rostral parts of the primary auditory field (A1). This progressed both in the approximate dorsoventral direction (along the isofrequency stripe) and in the rostrocaudal direction. The dorsal branch of the wavefront split into a caudal branch (propagating in A1) and another smaller one propagating rostrally into the AAF (anterior auditory field). After the front reached the caudal border of A1, a “reflection wave” appeared, propagating back rostrally. In total, the waves took ∼13–15 ms to propagate along A1 and return back. In CDCs, the propagation pattern was significantly disturbed, with a more synchronous activation of distant cortical regions. The maps obtained from contralateral and ipsilateral stimulation overlapped in both groups of animals. Although controls showed differences in the latency–amplitude patterns, cortical waves evoked by contralateral and ipsilateral stimulation were more similar in CDCs. Additionally, in controls, LFPs with contralateral and ipsilateral stimulation were more similar in caudal A1 than in rostral A1. This dichotomy was lost in deaf animals. In conclusion, propagating cortical waves are specific for the contralateral ear, they are affected by auditory deprivation, and the specificity of the cortex for stimulation of the contralateral ear is reduced by deprivation.

The Central Auditory System and Auditory Deprivation: Experience with Cochlear Implants in the Congenitally Deaf

In the present paper we briefly review the response of the central auditory system to auditory deprivation and describe recent experimental and clinical experience with cochlear implants. While the central auditory system undergoes marked changes in response to auditory deprivation, it would appear that at least a rudimentary cochleotopic organisation is maintained at the level of the brainstem and auditory cortex in animals deafened from birth. Moreover, recent studies have demonstrated the ability of the central auditory system to undergo functional reorganisation in response to changes in the pattern of afferent activity. Clinical experience has shown that deaf children with little or no prior auditory experience can obtain significant benefit from cochlear implants, provided the device is fitted at a young age. Furthermore, factors predicting successful clinical outcomes with these devices reflect the importance of auditory experience, either prior to an acquired loss or with the use of a cochlear implant. These findings suggest that functional reorganisation within the central auditory pathway can at least partially account for improvements in clinical performance over time.

Afferent projection patterns in the auditory brainstem in normal and congenitally deaf white cats.

Cochlear implantation in congenitally deaf children is developing to a successful medical tool. Little is known, however, on morphology and pathophysiology of the central auditory system in these auditory deprived children. One form of congenital hearing loss, that seen in the deaf white cat, was investigated to see if there are differences in the afferent pathways from the cochlear nuclei to the inferior colliculus. The retrogradely transported fluorescent tracer diamidino yellow (DY) was injected into different parts of the central nucleus of the inferior colliculus (ICC) of normal cats and deaf white cats. It was found that the main afferent projection patterns in deaf white cats were unchanged in spite of congenital auditory deprivation; minor differences were seen.

Unilateral hearing during development: hemispheric specificity in plastic reorganizations.

The present study investigates the hemispheric contributions of neuronal reorganization following early single-sided hearing (unilateral deafness). The experiments were performed on ten cats from our colony of deaf white cats. Two were identified in early hearing screening as unilaterally congenitally deaf. The remaining eight were bilaterally congenitally deaf, unilaterally implanted at different ages with a cochlear implant. Implanted animals were chronically stimulated using a single-channel portable signal processor for two to five months. Microelectrode recordings were performed at the primary auditory cortex under stimulation at the hearing and deaf ear with bilateral cochlear implants. Local field potentials (LFPs) were compared at the cortex ipsilateral and contralateral to the hearing ear. The focus of the study was on the morphology and the onset latency of the LFPs. With respect to morphology of LFPs, pronounced hemisphere-specific effects were observed. Morphology of amplitude-normalized LFPs for stimulation of the deaf and the hearing ear was similar for responses recorded at the same hemisphere. However, when comparisons were performed between the hemispheres, the morphology was more dissimilar even though the same ear was stimulated. This demonstrates hemispheric specificity of some cortical adaptations irrespective of the ear stimulated. The results suggest a specific adaptation process at the hemisphere ipsilateral to the hearing ear, involving specific (down-regulated inhibitory) mechanisms not found in the contralateral hemisphere. Finally, onset latencies revealed that the sensitive period for the cortex ipsilateral to the hearing ear is shorter than that for the contralateral cortex. Unilateral hearing experience leads to a functionally-asymmetric brain with different neuronal reorganizations and different sensitive periods involved.

Plastic Changes in the Auditory Cortex of Congenitally Deaf Cats following Cochlear Implantation

Congenitally deaf cats were used as a model for human inborn deafness and auditory deprivation. The deaf cats were supplied with a cochlear implant, chronically exposed to an acoustic environment and conditioned to acoustic stimuli. In case of early implantation the cats learned to make use of the newly gained auditory channel behaviourally. Neurophysiological and fMRI data showed that the central auditory system was recruited, if implantation took place within a sensitive period of <6 months.