Summary Progress in biomedical technology (cochlear, vestibular, and retinal implants) has led to remarkable success in neurosensory restoration, particularly in the auditory system. However, ...outcomes vary considerably, even after accounting for comorbidity—for example, after cochlear implantation, some deaf children develop spoken language skills approaching those of their hearing peers, whereas other children fail to do so. Here, we review evidence that auditory deprivation has widespread effects on brain development, affecting the capacity to process information beyond the auditory system. After sensory loss and deafness, the brain's effective connectivity is altered within the auditory system, between sensory systems, and between the auditory system and centres serving higher order neurocognitive functions. As a result, congenital sensory loss could be thought of as a connectome disease, with interindividual variability in the brain's adaptation to sensory loss underpinning much of the observed variation in outcome of cochlear implantation. Different executive functions, sequential processing, and concept formation are at particular risk in deaf children. A battery of clinical tests can allow early identification of neurocognitive risk factors. Intervention strategies that address these impairments with a personalised approach, taking interindividual variations into account, will further improve outcomes.
Deafness affects ∼2 in 1000 children and is one of the most common congenital impairments. Permanent hearing loss can be treated by fitting hearing aids. More severe to profound deafness is an ...indication for cochlear implantation. Although newborn hearing screening programs have increased the identification of asymmetric hearing loss, parents and caregivers of children with single-sided deafness are often hesitant to pursue therapy for the deaf ear. Delayed intervention has consequences for recovery of hearing. It has long been reported that asymmetric hearing loss/single-sided deafness compromises speech and language development and educational outcomes in children. Recent studies in animal models of deafness and in children consistently show evidence of an "aural preference syndrome" in which single-sided deafness in early childhood reorganizes the developing auditory pathways toward the hearing ear, with weaker central representation of the deaf ear. Delayed therapy consequently compromises benefit for the deaf ear, with slow rates of improvement measured over time. Therefore, asymmetric hearing needs early identification and intervention. Providing early effective stimulation in both ears through appropriate fitting of auditory prostheses, including hearing aids and cochlear implants, within a sensitive period in development has a cardinal role for securing the function of the impaired ear and for restoring binaural/spatial hearing. The impacts of asymmetric hearing loss on the developing auditory system and on spoken language development have often been underestimated. Thus, the traditional minimalist approach to clinical management aimed at 1 functional ear should be modified on the basis of current evidence.
Unilateral deafness has a high incidence in children. In addition to children who are born without hearing in one ear, children with bilateral deafness are frequently equipped only with one cochlear ...implant, leaving the other ear deaf. The present study investigates the effects of such single-sided deafness during development in the congenitally deaf cat. The investigated animals were either born with unilateral deafness or received a cochlear implant in one ear and were subjected to chronic monaural stimulation. In chronically stimulated animals, implantation ages were at the following three critical developmental points: "early" during the peak of functional cortical synaptogenesis in deaf animals; "intermediate" at the age when synaptic activity in the deaf cats dropped to the level of hearing control cats and finally, "late" at the age when the evoked synaptic activity fell below the level of hearing control cats. After periods of unilateral hearing, local field potentials were recorded from the cortical surface using a microelectrode at approximately 100 recording positions. Stimulation was with cochlear implants at both ears. The measures evaluated were dependent only on the symmetry of aural input: paired differences of onset latencies and paired relations of peak amplitudes of local field potentials. A massive reorganization of aural preference in favour of the hearing ear was found in these measures if the onset of unilateral hearing was early (before or around the peak of functional synaptogenesis). The effect was reduced if onset of unilateral hearing was in the intermediate period, and it disappeared if the onset was late. In early onset of unilateral deafness, the used ear became functionally dominant with respect to local field potential onset latency and amplitude. This explains the inferior outcome of implantations at the second-implanted ear compared with first-implanted ear in children. However, despite a central disadvantage for the deaf ear, it still remained capable of activating the auditory cortex. Appropriate training may thus help to improve the performance at the second-implanted ear. In conclusion, periods of monaural stimulation should be kept as short as possible, and training focused on the deaf ear should be introduced after delayed second implantation in children.
When the brain is deprived of input from one sensory modality, it often compensates with supranormal performance in one or more of the intact sensory systems. In the absence of acoustic input, it has ...been proposed that cross-modal reorganization of deaf auditory cortex may provide the neural substrate mediating compensatory visual function. We tested this hypothesis using a battery of visual psychophysical tasks and found that congenitally deaf cats, compared with hearing cats, have superior localization in the peripheral field and lower visual movement detection thresholds. In the deaf cats, reversible deactivation of posterior auditory cortex selectively eliminated superior visual localization abilities, whereas deactivation of the dorsal auditory cortex eliminated superior visual motion detection. Our results indicate that enhanced visual performance in the deaf is caused by cross-modal reorganization of deaf auditory cortex and it is possible to localize individual visual functions in discrete portions of reorganized auditory cortex.
Psychophysics and brain imaging studies in deaf patients have revealed a functional crossmodal reorganization that affects the remaining sensory modalities. Similarly, the congenital deaf cat (CDC) ...shows supra-normal visual skills that are supported by specific auditory fields (DZ-dorsal zone and P-posterior auditory cortex) but not the primary auditory cortex (A1). To assess the functional reorganization observed in deafness we analyzed the connectivity pattern of the auditory cortex by means of injections of anatomical tracers in DZ and A1 in both congenital deaf and normally hearing cats. A quantitative analysis of the distribution of the projecting neurons revealed the presence of non-auditory inputs to both A1 and DZ of the CDC which were not observed in the hearing cats. Firstly, some visual (areas 19/20) and somatosensory (SIV) areas were projecting toward DZ of the CDC but not in the control. Secondly, A1 of the deaf cat received a weak projection from the visual lateral posterior nuclei (LP). Most of these abnormal projections to A1 and DZ represent only a small fraction of the normal inputs to these areas. In addition, most of the afferents to DZ and A1 appeared normal in terms of areal specificity and strength of projection, with preserved but smeared nucleotopic gradient of A1 in CDCs. In conclusion, while the abnormal projections revealed in the CDC can participate in the crossmodal compensatory mechanisms, the observation of a limited reorganization of the connectivity pattern of the CDC implies that functional reorganization in congenital deafness is further supported also by normal cortico-cortical connectivity.
Electroacoustic stimulation in subjects with residual hearing is becoming more widely used in clinical practice. However, little is known about the properties of electrically induced responses in the ...hearing cochlea. In the present study, normal-hearing guinea pig cochleae underwent cochlear implantation through a cochleostomy without significant loss of hearing. Using recordings of unit activity in the midbrain, we were able to investigate the excitation patterns throughout the tonotopic field determined by acoustic stimulation. With the cochlear implant and the midbrain multielectrode arrays left in place, the ears were pharmacologically deafened and electrical stimulation was repeated in the deafened condition. The results demonstrate that, in addition to direct neuronal (electroneuronal) stimulation, in the hearing cochlea excitation of the hair cells occurs ("electrophonic responses") at the cochlear site corresponding to the dominant temporal frequency components of the electrical stimulus, provided these are < 12 kHz. The slope of the rate-level functions of the neurons in the deafened condition was steeper and the firing rate was higher than in the hearing condition at those sites that were activated in the two conditions. Finally, in a monopolar stimulation configuration, the differences between hearing status conditions were smaller than in the narrower (bipolar) configurations.
Stimulation with cochlear implants and hearing aids is becoming more widely clinically used in subjects with residual hearing. The neurophysiological characteristics underlying electroacoustic stimulation and the mechanism of its benefit remain unclear. The present study directly demonstrates that cochlear implantation does not interfere with the normal mechanical and physiological function of the cochlea. For the first time, it double-dissociates the electrical responses of hair cells (electrophonic responses) from responses of the auditory nerve fibers (electroneural responses), with separate excited cochlear locations in the same animals. We describe the condition in which these two responses spatially overlap. Finally, the study implicates that using the clinical characteristics of stimulation makes electrophonic responses unlikely in implanted subjects.
Cochlear variability is of key importance for the clinical use of cochlear implants, the most successful neuroprosthetic device that is surgically placed into the cochlear scala tympani. Despite ...extensive literature on human cochlear variability, few information is available on the variability of the modiolar wall. In the present study, we analyzed 108 corrosion casts, 95 clinical cone beam computer tomographies (CTs) and 15 µCTs of human cochleae and observed modiolar variability of similar and larger extent than the lateral wall variability. Lateral wall measures correlated with modiolar wall measures significantly. ~ 49% of the variability had a common cause. Based on these data we developed a model of the modiolar wall variations and related the model to the design of cochlear implants aimed for perimodiolar locations. The data demonstrate that both the insertion limits relevant for lateral wall damage (approximate range of 4-9 mm) as well as the dimensions required for optimal perimodiolar placement of the electrode (the point of release from the straightener; approximate range of 2-5mm) are highly interindividually variable. The data demonstrate that tip fold-overs of preformed implants likely result from the morphology of the modiolus (with radius changing from base to apex), and that optimal cochlear implantation of perimodiolar arrays cannot be guaranteed without an individualized surgical technique.
Intracochlear optical stimulation has been suggested as an alternative approach to hearing prosthetics in recent years. This study investigated the properties of a near infrared laser (NIR) induced ...optoacoustic effect. Pressure recordings were performed at the external meatus of anaesthetized guinea pigs during intracochlear NIR stimulation. The sound pressure and power spectra were determined. The results were compared to multi unit responses in the inferior colliculus (IC). Additionally, the responses to NIR stimulation were compared to IC responses induced by intracochlear electric stimulation at the same cochlear position to investigate a potentially confounding contribution of direct neural NIR stimulation. The power spectra of the sound recorded at the external meatus (n = 7) had most power at frequencies below 10 kHz and showed little variation for different stimulation sites. The mean spike rates of IC units responding to intracochlear NIR stimulation (n = 222) of 17 animals were significantly correlated with the power of the externally recorded signal at frequencies corresponding to the best frequencies of the IC units. The response strength as well as the sound pressure at the external meatus depended on the pulse peak power of the optical stimulus. The sound pressure recorded at the external meatus reached levels above 70 dB SPL peak equivalent. In hearing animals a cochlear activation apical to the location of the fiber was found. The absence of any NIR responses after pharmacologically deafening and the comparison to electric stimulation at the NIR stimulation site revealed no indication of a confounding direct neural NIR stimulation. Intracochlear optoacoustic stimulation might become useful in combined electro-acoustic stimulation devices in the future.
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•Sound can be recorded at the external meatus during intracochlear laser stimulation.•The power spectrum fits to the neural response pattern in the inferior colliculus.•Response maxima occur below 10 kHz.•No responses could be recorded after deafening.•Optoacoustic stimulation may be suitable for implantable hearing aids.
Environmental events often occur on a probabilistic basis but can sometimes be predicted based on specific cues and thus approached proactively. Incidental statistical learning enables the ...acquisition of knowledge about probabilistic cue-target contingencies. However, the neural mechanisms of statistical learning about contingencies (SLC), the required conditions for successful learning, and the role of implicit processes in the resultant proactive behavior are still debated. We examined changes in behavior and cortical activity during an SLC task in which subjects responded to visual targets. Unbeknown to them, there were three types of target cues associated with high-, low-, and zero target probabilities. About half of the subjects spontaneously gained explicit knowledge about the contingencies (contingency-aware group), and only they showed evidence of proactivity: shortened response times to predictable targets and enhanced event-related brain responses (cue-evoked P300 and contingent negative variation, CNV) to high probability cues. The behavioral and brain responses were strictly associated on a single-trial basis. Source reconstruction of the brain responses revealed activation of fronto-parietal brain regions associated with cognitive control, particularly the anterior cingulate cortex and precuneus. We also found neural correlates of SLC in the contingency-unaware group, but these were restricted to post-target latencies and visual association areas. Our results document a qualitative difference between explicit and implicit learning processes and suggest that in certain conditions, proactivity may require explicit knowledge about contingencies.
Congenital deafness leads to functional deficits in the auditory cortex for which early cochlear implantation can effectively compensate. Most of these deficits have been demonstrated functionally. ...Furthermore, the majority of previous studies on deafness have involved the primary auditory cortex; knowledge of higher‐order areas is limited to effects of cross‐modal reorganization. In this study, we compared the cortical cytoarchitecture of four cortical areas in adult hearing and congenitally deaf cats (CDCs): the primary auditory field A1, two secondary auditory fields, namely the dorsal zone and second auditory field (A2); and a reference visual association field (area 7) in the same section stained either using Nissl or SMI‐32 antibodies. The general cytoarchitectonic pattern and the area‐specific characteristics in the auditory cortex remained unchanged in animals with congenital deafness. Whereas area 7 did not differ between the groups investigated, all auditory fields were slightly thinner in CDCs, this being caused by reduced thickness of layers IV–VI. The study documents that, while the cytoarchitectonic patterns are in general independent of sensory experience, reduced layer thickness is observed in both primary and higher‐order auditory fields in layer IV and infragranular layers. The study demonstrates differences in effects of congenital deafness between supragranular and other cortical layers, but similar dystrophic effects in all investigated auditory fields.
Cytoarchitectonics in primary and higher‐order auditory cortical areas was not affected by congenital auditory deprivation (deafness). Reduced layer thickness in deep cortical layers IV–VI of primary and higher‐order areas was observed, despite cross‐modal reorganization in some of them. Cross‐modal reorganization did not protect the cortex from dystrophic changes.
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