Cortical imbalance following delayed restoration of bilateral hearing in deaf adolescents.

Unilateral auditory deprivation in early childhood can lead to cortical strengthening of inputs from the stimulated side, yet the impact of this on bilateral processing when inputs are later restored beyond an early sensitive period is unknown. To address this, we conducted a longitudinal study with 13 bilaterally profoundly deaf adolescents who received unilateral access to sound via a cochlear implant (CI) in their right ear in early childhood before receiving bilateral access to sound a decade later via a second CI in their left ear. Auditory-evoked cortical responses to unilateral and bilateral stimulation were measured repeatedly using electroencephalogram from 1 week to 14 months after activation of their second CI. Early cortical responses from the newly implanted ear and bilateral stimulation were atypically lateralized to the left ipsilateral auditory cortex. Duration of unilateral deafness predicted an unexpectedly stronger representation of inputs from the newly implanted, compared to the first implanted ear, in left auditory cortex. Significant initial reductions in responses were observed, yet a left-hemisphere bias and unequal weighting of inputs favoring the long-term deaf ear did not converge to a balanced state observed in the binaurally developed system. Bilateral response enhancement was significantly reduced in left auditory cortex suggesting deficits in ipsilateral response inhibition of new, dominant, inputs during bilateral processing. These findings paradoxically demonstrate the adaptive capacity of the adolescent auditory system beyond an early sensitive period for bilateral input, as well as restrictions on its potential to fully reverse cortical imbalances driven by long-term unilateral deafness.

Adaptive benefit of cross-modal plasticity following cochlear implantation in deaf adults.

It has been suggested that visual language is maladaptive for hearing restoration with a cochlear implant (CI) due to cross-modal recruitment of auditory brain regions. Rehabilitative guidelines therefore discourage the use of visual language. However, neuroscientific understanding of cross-modal plasticity following cochlear implantation has been restricted due to incompatibility between established neuroimaging techniques and the surgically implanted electronic and magnetic components of the CI. As a solution to this problem, here we used functional near-infrared spectroscopy (fNIRS), a noninvasive optical neuroimaging method that is fully compatible with a CI and safe for repeated testing. The aim of this study was to examine cross-modal activation of auditory brain regions by visual speech from before to after implantation and its relation to CI success. Using fNIRS, we examined activation of superior temporal cortex to visual speech in the same profoundly deaf adults both before and 6 mo after implantation. Patients' ability to understand auditory speech with their CI was also measured following 6 mo of CI use. Contrary to existing theory, the results demonstrate that increased cross-modal activation of auditory brain regions by visual speech from before to after implantation is associated with better speech understanding with a CI. Furthermore, activation of auditory cortex by visual and auditory speech developed in synchrony after implantation. Together these findings suggest that cross-modal plasticity by visual speech does not exert previously assumed maladaptive effects on CI success, but instead provides adaptive benefits to the restoration of hearing after implantation through an audiovisual mechanism.

Investigating Cortical Responses to Noise-Vocoded Speech in Children with Normal Hearing Using Functional Near-Infrared Spectroscopy (fNIRS).

Whilst functional neuroimaging has been used to investigate cortical processing of degraded speech in adults, much less is known about how these signals are processed in children. An enhanced understanding of cortical correlates of poor speech perception in children would be highly valuable to oral communication applications, including hearing devices. We utilised vocoded speech stimuli to investigate brain responses to degraded speech in 29 normally hearing children aged 6-12 years. Intelligibility of the speech stimuli was altered in two ways by (i) reducing the number of spectral channels and (ii) reducing the amplitude modulation depth of the signal. A total of five different noise-vocoded conditions (with zero, partial or high intelligibility) were presented in an event-related format whilst participants underwent functional near-infrared spectroscopy (fNIRS) neuroimaging. Participants completed a word recognition task during imaging, as well as a separate behavioural speech perception assessment. fNIRS recordings revealed statistically significant sensitivity to stimulus intelligibility across several brain regions. More intelligible stimuli elicited stronger responses in temporal regions, predominantly within the left hemisphere, while right inferior parietal regions showed an opposite, negative relationship. Although there was some evidence that partially intelligible stimuli elicited the strongest responses in the left inferior frontal cortex, a region previous studies have suggested is associated with effortful listening in adults, this effect did not reach statistical significance. These results further our understanding of cortical mechanisms underlying successful speech perception in children. Furthermore, fNIRS holds promise as a clinical technique to help assess speech intelligibility in paediatric populations.

The Benefit of Cross-Modal Reorganization on Speech Perception in Pediatric Cochlear Implant Recipients Revealed Using Functional Near-Infrared Spectroscopy.

Cochlear implants (CIs) are the most successful treatment for severe-to-profound deafness in children. However, speech outcomes with a CI often lag behind those of normally-hearing children. Some authors have attributed these deficits to the takeover of the auditory temporal cortex by vision following deafness, which has prompted some clinicians to discourage the rehabilitation of pediatric CI recipients using visual speech. We studied this cross-modal activity in the temporal cortex, along with responses to auditory speech and non-speech stimuli, in experienced CI users and normally-hearing controls of school-age, using functional near-infrared spectroscopy. Strikingly, CI users displayed significantly greater cortical responses to visual speech, compared with controls. Importantly, in the same regions, the processing of auditory speech, compared with non-speech stimuli, did not significantly differ between the groups. This suggests that visual and auditory speech are processed synergistically in the temporal cortex of children with CIs, and they should be encouraged, rather than discouraged, to use visual speech.

Pre-operative Brain Imaging Using Functional Near-Infrared Spectroscopy Helps Predict Cochlear Implant Outcome in Deaf Adults.

Currently, it is not possible to accurately predict how well a deaf individual will be able to understand speech when hearing is (re)introduced via a cochlear implant. Differences in brain organisation following deafness are thought to contribute to variability in speech understanding with a cochlear implant and may offer unique insights that could help to more reliably predict outcomes. An emerging optical neuroimaging technique, functional near-infrared spectroscopy (fNIRS), was used to determine whether a pre-operative measure of brain activation could explain variability in cochlear implant (CI) outcomes and offer additional prognostic value above that provided by known clinical characteristics. Cross-modal activation to visual speech was measured in bilateral superior temporal cortex of pre- and post-lingually deaf adults before cochlear implantation. Behavioural measures of auditory speech understanding were obtained in the same individuals following 6 months of cochlear implant use. The results showed that stronger pre-operative cross-modal activation of auditory brain regions by visual speech was predictive of poorer auditory speech understanding after implantation. Further investigation suggested that this relationship may have been driven primarily by the inclusion of, and group differences between, pre- and post-lingually deaf individuals. Nonetheless, pre-operative cortical imaging provided additional prognostic value above that of influential clinical characteristics, including the age-at-onset and duration of auditory deprivation, suggesting that objectively assessing the physiological status of the brain using fNIRS imaging pre-operatively may support more accurate prediction of individual CI outcomes. Whilst activation of auditory brain regions by visual speech prior to implantation was related to the CI user's clinical history of deafness, activation to visual speech did not relate to the future ability of these brain regions to respond to auditory speech stimulation with a CI. Greater pre-operative activation of left superior temporal cortex by visual speech was associated with enhanced speechreading abilities, suggesting that visual speech processing may help to maintain left temporal lobe specialisation for language processing during periods of profound deafness.

Evaluating time-reversed speech and signal-correlated noise as auditory baselines for isolating speech-specific processing using fNIRS.

Evidence using well-established imaging techniques, such as functional magnetic resonance imaging and electrocorticography, suggest that speech-specific cortical responses can be functionally localised by contrasting speech responses with an auditory baseline stimulus, such as time-reversed (TR) speech or signal-correlated noise (SCN). Furthermore, these studies suggest that SCN is a more effective baseline than TR speech. Functional near-infrared spectroscopy (fNIRS) is a relatively novel, optically-based imaging technique with features that make it ideal for investigating speech and language function in paediatric populations. However, it is not known which baseline is best at isolating speech activation when imaging using fNIRS. We presented normal speech, TR speech and SCN in an event-related format to 25 normally-hearing children aged 6-12 years. Brain activity was measured across frontal and temporal brain areas in both cerebral hemispheres whilst children passively listened to the auditory stimuli. In all three conditions, significant activation was observed bilaterally in channels targeting superior temporal regions when stimuli were contrasted against silence. Unlike previous findings in infants, we found no significant activation in the region of interest over superior temporal cortex in school-age children when normal speech was contrasted against either TR speech or SCN. Although no statistically significant lateralisation effects were observed in the region of interest, a left-sided channel targeting posterior temporal regions showed significant activity in response to normal speech only, and was investigated further. Significantly greater activation was observed in this left posterior channel compared to the corresponding channel on the right side under the normal speech vs SCN contrast only. Our findings suggest that neither TR speech nor SCN are suitable auditory baselines for functionally isolating speech-specific processing in an experimental set up involving fNIRS with 6-12 year old children.

Cortical correlates of speech intelligibility measured using functional near-infrared spectroscopy (fNIRS).

Functional neuroimaging has identified that the temporal, frontal and parietal cortex support core aspects of speech processing. An objective measure of speech intelligibility based on cortical activation in these brain regions would be extremely useful to speech communication and hearing device applications. In the current study, we used noise-vocoded speech to examine cortical correlates of speech intelligibility in normally-hearing listeners using functional near-infrared spectroscopy (fNIRS), a non-invasive, neuroimaging technique that is fully-compatible with hearing devices, including cochlear implants. In twenty-three normally-hearing adults we measured (1) activation in superior temporal, inferior frontal and inferior parietal cortex bilaterally and (2) behavioural speech intelligibility. Listeners heard noise-vocoded sentences targeting five equally spaced levels of intelligibility between 0 and 100% correct. Activation in superior temporal regions increased linearly with intelligibility. This relationship appears to have been driven in part by changing acoustic properties across stimulation conditions, rather than solely by intelligibility per se. Superior temporal activation was also predictive of individual differences in intelligibility in a challenging listening condition. Beyond superior temporal cortex, we identified regions in which activation varied non-linearly with intelligibility. For example, in left inferior frontal cortex, activation peaked in response to heavily degraded, yet still somewhat intelligible, speech. Activation in this region was linearly related to response time on a simultaneous behavioural task, suggesting it may contribute to decision making. Our results indicate that fNIRS has the potential to provide an objective measure of speech intelligibility in normally-hearing listeners. Should these results be found to apply similarly in the case of individuals listening through a cochlear implant, fNIRS would demonstrate potential for a clinically useful measure not only of speech intelligibility, but also of listening effort.

Plasticity in bilateral superior temporal cortex: Effects of deafness and cochlear implantation on auditory and visual speech processing.

While many individuals can benefit substantially from cochlear implantation, the ability to perceive and understand auditory speech with a cochlear implant (CI) remains highly variable amongst adult recipients. Importantly, auditory performance with a CI cannot be reliably predicted based solely on routinely obtained information regarding clinical characteristics of the CI candidate. This review argues that central factors, notably cortical function and plasticity, should also be considered as important contributors to the observed individual variability in CI outcome. Superior temporal cortex (STC), including auditory association areas, plays a crucial role in the processing of auditory and visual speech information. The current review considers evidence of cortical plasticity within bilateral STC, and how these effects may explain variability in CI outcome. Furthermore, evidence of audio-visual interactions in temporal and occipital cortices is examined, and relation to CI outcome is discussed. To date, longitudinal examination of changes in cortical function and plasticity over the period of rehabilitation with a CI has been restricted by methodological challenges. The application of functional near-infrared spectroscopy (fNIRS) in studying cortical function in CI users is becoming increasingly recognised as a potential solution to these problems. Here we suggest that fNIRS offers a powerful neuroimaging tool to elucidate the relationship between audio-visual interactions, cortical plasticity during deafness and following cochlear implantation, and individual variability in auditory performance with a CI.

Speech-evoked activation in adult temporal cortex measured using functional near-infrared spectroscopy (fNIRS): Are the measurements reliable?

Functional near-infrared spectroscopy (fNIRS) is a silent, non-invasive neuroimaging technique that is potentially well suited to auditory research. However, the reliability of auditory-evoked activation measured using fNIRS is largely unknown. The present study investigated the test-retest reliability of speech-evoked fNIRS responses in normally-hearing adults. Seventeen participants underwent fNIRS imaging in two sessions separated by three months. In a block design, participants were presented with auditory speech, visual speech (silent speechreading), and audiovisual speech conditions. Optode arrays were placed bilaterally over the temporal lobes, targeting auditory brain regions. A range of established metrics was used to quantify the reproducibility of cortical activation patterns, as well as the amplitude and time course of the haemodynamic response within predefined regions of interest. The use of a signal processing algorithm designed to reduce the influence of systemic physiological signals was found to be crucial to achieving reliable detection of significant activation at the group level. For auditory speech (with or without visual cues), reliability was good to excellent at the group level, but highly variable among individuals. Temporal-lobe activation in response to visual speech was less reliable, especially in the right hemisphere. Consistent with previous reports, fNIRS reliability was improved by averaging across a small number of channels overlying a cortical region of interest. Overall, the present results confirm that fNIRS can measure speech-evoked auditory responses in adults that are highly reliable at the group level, and indicate that signal processing to reduce physiological noise may substantially improve the reliability of fNIRS measurements.