Language networks of normal-hearing infants exhibit topological differences between resting and steady states: An fNIRS functional connectivity study.

Task-related studies have consistently reported that listening to speech sounds activate the temporal and prefrontal regions of the brain. However, it is not well understood how functional organization of auditory and language networks differ when processing speech sounds from its resting state form. The knowledge of language network organization in typically developing infants could serve as an important biomarker to understand network-level disruptions expected in infants with hearing impairment. We hypothesized that topological differences of language networks can be characterized using functional connectivity measures in two experimental conditions (1) complete silence (resting) and (2) in response to repetitive continuous speech sounds (steady). Thirty normal-hearing infants (14 males and 16 females, age: 7.8 ± 4.8 months) were recruited in this study. Brain activity was recorded from bilateral temporal and prefrontal regions associated with speech and language processing for two experimental conditions: resting and steady states. Topological differences of functional language networks were characterized using graph theoretical analysis. The normalized global efficiency and clustering coefficient were used as measures of functional integration and segregation, respectively. We found that overall, language networks of infants demonstrate the economic small-world organization in both resting and steady states. Moreover, language networks exhibited significantly higher functional integration and significantly lower functional segregation in resting state compared to steady state. A secondary analysis that investigated developmental effects of infants aged 6-months or below and above 6-months revealed that such topological differences in functional integration and segregation across resting and steady states can be reliably detected after the first 6-months of life. The higher functional integration observed in resting state suggests that language networks of infants facilitate more efficient parallel information processing across distributed language regions in the absence of speech stimuli. Moreover, higher functional segregation in steady state indicates that the speech information processing occurs within densely interconnected specialized regions in the language network.

Resting-State Functional Connectivity Predicts Cochlear-Implant Speech Outcomes.

OBJECTIVES: Cochlear implants (CIs) have revolutionized hearing restoration for individuals with severe or profound hearing loss. However, a substantial and unexplained variability persists in CI outcomes, even when considering subject-specific factors such as age and the duration of deafness. In a pioneering study, we use resting-state functional near-infrared spectroscopy to predict speech-understanding outcomes before and after CI implantation. Our hypothesis centers on resting-state functional connectivity (FC) reflecting brain plasticity post-hearing loss and implantation, specifically targeting the average clustering coefficient in resting FC networks to capture variation among CI users. DESIGN: Twenty-three CI candidates participated in this study. Resting-state functional near-infrared spectroscopy data were collected preimplantation and at 1 month, 3 months, and 1 year postimplantation. Speech understanding performance was assessed using consonant-nucleus-consonant words in quiet and Bamford-Kowal-Bench sentences in noise 1-year postimplantation. Resting-state FC networks were constructed using regularized partial correlation, and the average clustering coefficient was measured in the signed weighted networks as a predictive measure for implantation outcomes. RESULTS: Our findings demonstrate a significant correlation between the average clustering coefficient in resting-state functional networks and speech understanding outcomes, both pre- and postimplantation. CONCLUSIONS: This approach uses an easily deployable resting-state functional brain imaging metric to predict speech-understanding outcomes in implant recipients. The results indicate that the average clustering coefficient, both pre- and postimplantation, correlates with speech understanding outcomes.

The Use of Heart Rate Responses Extracted From Functional Near-Infrared Spectroscopy Data as a Measure of Speech Discrimination Ability in Sleeping Infants.

OBJECTIVES: Cardiac responses (e.g., heart rate changes) due to an autonomous response to sensory stimuli have been reported in several studies. This study investigated whether heart rate information extracted from functional near-infrared spectroscopy (fNIRS) data can be used to assess the discrimination of speech sounds in sleeping infants. This study also investigated the adaptation of the heart rate response over multiple, sequential stimulus presentations. DESIGN: fNIRS data were recorded from 23 infants with no known hearing loss, aged 2 to 10 months. Speech syllables were presented using a habituation/dishabituation test paradigm: the infant's heart rate response was first habituated by repeating blocks of one speech sound; then, the heart rate response was dishabituated with the contrasting (novel) speech sound. This stimulus presentation sequence was repeated for as long as the infants were asleep. RESULTS: The group-level average heart rate response to the novel stimulus was greater than that to the habituated first sound, indicating that sleeping infants were able to discriminate the speech sound contrast. A significant adaptation of the heart rate responses was seen over the session duration. CONCLUSION: The dishabituation response could be a valuable marker for speech discrimination, especially when used in conjunction with the fNIRS hemodynamic response.

Development of an Australian behavioural method for assessing listening task difficulty at high speech intelligibility levels.

OBJECTIVE: To develop and validate an Australian version of a behavioural test for assessing listening task difficulty at high speech intelligibility levels. DESIGN: In the SWIR-Aus test, listeners perform two tasks: identify the last word of each of seven sentences in a list and recall the identified words after each list. First, the test material was developed by creating seven-sentence lists with similar final-word features. Then, for the validation, participant's performance on the SWIR-Aus test was compared when a binary mask noise reduction algorithm was on and off. STUDY SAMPLE: All participants in this study had normal hearing thresholds. Nine participants (23.8-56.0 years) participated in the characterisation of the speech material. Another thirteen participants (18.4-59.1 years) participated in a pilot test to determine the SNR to use at the validation stage. Finally, twenty-four new participants (20.0-56.9 years) participated in the validation of the test. RESULTS: The results of the validation of the test showed that recall and identification scores were significantly better when the binary mask noise reduction algorithm was on compared to off. CONCLUSIONS: The SWIR-Aus test was developed using Australian speech material and can be used for assessing task difficulty at high speech intelligibility levels.

Audio-visual integration in cochlear implant listeners and the effect of age difference.

This study aimed to investigate differences in audio-visual (AV) integration between cochlear implant (CI) listeners and normal-hearing (NH) adults. A secondary aim was to investigate the effect of age differences by examining AV integration in groups of older and younger NH adults. Seventeen CI listeners, 13 similarly aged NH adults, and 16 younger NH adults were recruited. Two speech identification experiments were conducted to evaluate AV integration of speech cues. In the first experiment, reaction times in audio-alone (A-alone), visual-alone (V-alone), and AV conditions were measured during a speeded task in which participants were asked to identify a target sound /aSa/ among 11 alternatives. A race model was applied to evaluate AV integration. In the second experiment, identification accuracies were measured using a closed set of consonants and an open set of consonant-nucleus-consonant words. The authors quantified AV integration using a combination of a probability model and a cue integration model (which model participants' AV accuracy by assuming no or optimal integration, respectively). The results found that experienced CI listeners showed no better AV integration than their similarly aged NH adults. Further, there was no significant difference in AV integration between the younger and older NH adults.

The effect of presentation level and stimulation rate on speech perception and modulation detection for cochlear implant users.

In order to improve speech understanding for cochlear implant users, it is important to maximize the transmission of temporal information. The combined effects of stimulation rate and presentation level on temporal information transfer and speech understanding remain unclear. The present study systematically varied presentation level (60, 50, and 40 dBA) and stimulation rate [500 and 2400 pulses per second per electrode (pps)] in order to observe how the effect of rate on speech understanding changes for different presentation levels. Speech recognition in quiet and noise, and acoustic amplitude modulation detection thresholds (AMDTs) were measured with acoustic stimuli presented to speech processors via direct audio input (DAI). With the 500 pps processor, results showed significantly better performance for consonant-vowel nucleus-consonant words in quiet, and a reduced effect of noise on sentence recognition. However, no rate or level effect was found for AMDTs, perhaps partly because of amplitude compression in the sound processor. AMDTs were found to be strongly correlated with the effect of noise on sentence perception at low levels. These results indicate that AMDTs, at least when measured with the CP910 Freedom speech processor via DAI, explain between-subject variance of speech understanding, but do not explain within-subject variance for different rates and levels.

Connectivity in Language Areas of the Brain in Cochlear Implant Users as Revealed by fNIRS.

Many studies, using a variety of imaging techniques, have shown that deafness induces functional plasticity in the brain of adults with late-onset deafness, and in children changes the way the auditory brain develops. Cross modal plasticity refers to evidence that stimuli of one modality (e.g. vision) activate neural regions devoted to a different modality (e.g. hearing) that are not normally activated by those stimuli. Other studies have shown that multimodal brain networks (such as those involved in language comprehension, and the default mode network) are altered by deafness, as evidenced by changes in patterns of activation or connectivity within the networks. In this paper, we summarise what is already known about brain plasticity due to deafness and propose that functional near-infra-red spectroscopy (fNIRS) is an imaging method that has potential to provide prognostic and diagnostic information for cochlear implant users. Currently, patient history factors account for only 10 % of the variation in post-implantation speech understanding, and very few post-implantation behavioural measures of hearing ability correlate with speech understanding. As a non-invasive, inexpensive and user-friendly imaging method, fNIRS provides an opportunity to study both pre- and post-implantation brain function. Here, we explain the principle of fNIRS measurements and illustrate its use in studying brain network connectivity and function with example data.

Electrode Selection and Speech Understanding in Patients With Auditory Brainstem Implants.

OBJECTIVES: The objective of this study was to evaluate whether speech understanding in auditory brainstem implant (ABI) users who have a tumor pathology could be improved by the selection of a subset of electrodes that were appropriately pitch ranked and distinguishable. It was hypothesized that disordered pitch or spectral percepts and channel interactions may contribute significantly to the poor outcomes in most ABI users. DESIGN: A single-subject design was used with five participants. Pitch ranking information for all electrodes in the patients' clinic maps was obtained using a pitch ranking task and previous pitch ranking information from clinic sessions. A multidimensional scaling task was used to evaluate the stimulus space evoked by stimuli on the same set of electrodes. From this information, a subset of four to six electrodes was chosen and a new map was created, using just this subset, that the subjects took home for 1 month's experience. Closed-set consonant and vowel perception and sentences in quiet were tested at three sessions: with the clinic map before the test map was given, after 1 month with the test map, and after an additional 2 weeks with their clinic map. RESULTS: The results of the pitch ranking and multidimensional scaling procedures confirmed that the ABI users did not have a well-ordered set of percepts related to electrode position, thus supporting the proposal that difficulty in processing of spectral information may contribute to poor speech understanding. However, none of the subjects benefited from a map that reduced the stimulation electrode set to a smaller number of electrodes that were well ordered in place pitch. CONCLUSIONS: Although poor spectral processing may contribute to poor understanding in ABI users, it is not likely to be the sole contributor to poor outcomes.

The perception of complex pitch in cochlear implants: A comparison of monopolar and tripolar stimulation.

Cochlear implant listeners typically perform poorly in tasks of complex pitch perception (e.g., musical pitch and voice pitch). One explanation is that wide current spread during implant activation creates channel interactions that may interfere with perception of temporal fundamental frequency information contained in the amplitude modulations within channels. Current focusing using a tripolar mode of stimulation has been proposed as a way of reducing channel interactions, minimising spread of excitation and potentially improving place and temporal pitch cues. The present study evaluated the effect of mode in a group of cochlear implant listeners on a pitch ranking task using male and female singing voices separated by either a half or a quarter octave. Results were variable across participants, but on average, pitch ranking was at chance level when the pitches were a quarter octave apart and improved when the difference was a half octave. No advantage was observed for tripolar over monopolar mode at either pitch interval, suggesting that previously published psychophysical advantages for focused modes may not translate into improvements in complex pitch ranking. Evaluation of the spectral centroid of the stimulation pattern, plus a lack of significant difference between male and female voices, suggested that participants may have had difficulty in accessing temporal pitch cues in either mode.

Effect of input compression and input frequency response on music perception in cochlear implant users.

OBJECTIVE: A study was conducted to determine whether modifications to input compression and input frequency response characteristics can improve music-listening satisfaction in cochlear implant users. DESIGN: Experiment 1 compared three pre-processed versions of music and speech stimuli in a laboratory setting: original, compressed, and flattened frequency response. Music excerpts comprised three music genres (classical, country, and jazz), and a running speech excerpt was compared. Experiment 2 implemented a flattened input frequency response in the speech processor program. In a take-home trial, participants compared unaltered and flattened frequency responses. STUDY SAMPLE: Ten and twelve adult Nucleus Freedom cochlear implant users participated in Experiments 1 and 2, respectively. RESULTS: Experiment 1 revealed a significant preference for music stimuli with a flattened frequency response compared to both original and compressed stimuli, whereas there was a significant preference for the original (rising) frequency response for speech stimuli. Experiment 2 revealed no significant mean preference for the flattened frequency response, with 9 of 11 subjects preferring the rising frequency response. CONCLUSIONS: Input compression did not alter music enjoyment. Comparison of the two experiments indicated that individual frequency response preferences may depend on the genre or familiarity, and particularly whether the music contained lyrics.

Processing of speech temporal and spectral information by users of auditory brainstem implants and cochlear implants.

OBJECTIVES: Auditory brainstem implants (ABI) use the same processing strategy as was developed for cochlear implants (CI). However, the cochlear nucleus (CN), the stimulation site of ABIs, is anatomically and physiologically more complex than the auditory nerve and consists of neurons with differing roles in auditory processing. The aim of this study was to evaluate the hypotheses that ABI users are less able than CI users to access speech spectro-temporal information delivered by the existing strategies and that the sites stimulated by different locations of CI and ABI electrode arrays differ in encoding of temporal patterns in the stimulation. DESIGN: Six CI users and four ABI users of Nucleus implants with ACE processing strategy participated in this study. Closed-set perception of aCa syllables (16 consonants) and bVd words (11 vowels) was evaluated via experimental processing strategies that activated one, two, or four of the electrodes of the array in a CIS manner as well as subjects' clinical strategies. Three single-channel strategies presented the overall temporal envelope variations of the signal on a single-implant electrode located at the high-, medium-, and low-frequency regions of the array. Implantees' ability to discriminate within electrode temporal patterns of stimulation for phoneme perception and their ability to make use of spectral information presented by increased number of active electrodes were assessed in the single- and multiple-channel strategies, respectively. Overall percentages and information transmission of phonetic features were obtained for each experimental program. RESULTS: Phoneme perception performance of three ABI users was within the range of CI users in most of the experimental strategies and improved as the number of active electrodes increased. One ABI user performed close to chance with all the single and multiple electrode strategies. There was no significant difference between apical, basal, and middle CI electrodes in transmitting speech temporal information, except a trend that the voicing feature was the least transmitted by the basal electrode. A similar electrode-location pattern could be observed in most ABI subjects. CONCLUSIONS: Although the number of tested ABI subjects was small, their wide range of phoneme perception performance was consistent with previous reports of overall speech perception in ABI patients. The better-performing ABI user participants had access to speech temporal and spectral information that was comparable to that of average CI user. The poor-performing ABI user did not have access to within-channel speech temporal information and did not benefit from an increased number of spectral channels. The within-subject variability between different ABI electrodes was less than the variability across users in transmission of speech temporal information. The difference in the performance of ABI users could be related to the location of their electrode array on the CN, anatomy, and physiology of their CN or the damage to their auditory brainstem due to tumor or surgery.

Estimating confidence intervals for information transfer analysis of confusion matrices.

A non-parametric bootstrapping statistical method is introduced and investigated for estimating confidence intervals resulting from information transfer (IT) analysis of confusion matrices. Confidence intervals can be used to statistically compare ITs from two or more confusion matrices obtained in an experiment. Information transfer is a nonlinear analysis and does not satisfy many of the assumptions of a parametric method. The bootstrapping method accurately estimated IT confidence intervals as long as the confusion matrices contained a sufficiently large number of presentations per stimulus category, which is also a condition for reduced bias in IT analysis.

Interpulse interval discrimination within and across channels: comparison of monopolar and tripolar mode of stimulation.

Perception of temporal patterns is crucial to speech understanding and music perception in normal hearing, and is fundamental in the design and implementation of processing strategies for cochlear implants. Two experiments described here investigated the effect of stimulation mode (monopolar versus tripolar) on interpulse interval discrimination using single-electrode stimulation (experiment 1) and dual-electrode stimulation (experiment 2). Experiment 1 required participants to discriminate stimuli containing different interpulse intervals and experiment 2 required listeners to discriminate between two dual-electrode stimuli that had the same temporal pattern on each electrode, but differed in inter-electrode timing. The hypotheses were that (i) stimulation mode would affect the ability to distinguish interpulse interval patterns on a single electrode and (ii) the electrode separation range in which subjects were sensitive to inter-electrode timing would be more restricted in tripolar than in monopolar stimulation. Results in nine cochlear implant users showed that mode did not have a significant mean effect on either the ability to discriminate interpulse intervals in single-electrode stimulation or the range of electrode separation in dual-electrode stimulation in which participants were sensitive to inter-electrode timing. In conclusion, tripolar stimulation did not show any advantage in delivering temporal information within or across channels in this group.

Loudness of time-varying stimuli with electric stimulation.

McKay, Henshall, Farrell, and McDermott [J. Acoust. Soc. Am. 113, 2054-2063 (2003)] developed a practical method to estimate the loudness of periodic electrical signals presented through a cochlear implant. In the present work, this method was extended to time-varying sounds based on two models of time-varying loudness for normal listeners. To fit the model parameters, loudness balancing data was collected with six cochlear implant listeners. The pulse rate of a modulated pulse train was adjusted to equalize its loudness to a reference stimulus. The stimuli were single-electrode time-limited pulse bursts, repeated at a rate of 50 Hz, with on-times varying between 2 and 20 ms. The parameters of two different models of time-varying loudness were fitted to the results. For each model, parameters defining the time windows over which the electrical pulses contribute to instantaneous loudness were optimized. In each case, a good fit was obtained with the loudness balancing results. Therefore, the practical method was successfully extended to time-varying sounds by combining it with existing models of time-varying loudness for acoustic stimulation.

Two Independent Response Mechanisms to Auditory Stimuli Measured with Functional Near-Infrared Spectroscopy in Sleeping Infants.

This study investigated the morphology of the functional near-infrared spectroscopy (fNIRS) response to speech sounds measured from 16 sleeping infants and how it changes with repeated stimulus presentation. We observed a positive peak followed by a wide negative trough, with the latter being most evident in early epochs. We argue that the overall response morphology captures the effects of two simultaneous, but independent, response mechanisms that are both activated at the stimulus onset: one being the obligatory response to a sound stimulus by the auditory system, and the other being a neural suppression effect induced by the arousal system. Because the two effects behave differently with repeated epochs, it is possible to mathematically separate them and use fNIRS to study factors that affect the development and activation of the arousal system in infants. The results also imply that standard fNIRS analysis techniques need to be adjusted to take into account the possibilities of multiple simultaneous brain systems being activated and that the response to a stimulus is not necessarily stationary.

Place specificity measured in forward and interleaved masking in cochlear implants.

Interleaved masking in cochlear implants is analogous to acoustic simultaneous masking and is relevant to speech processing strategies that interleave pulses on concurrently activated electrodes. In this study, spatial decay of masking as the distance between masker and probe increases was compared between forward and interleaved masking in the same group of cochlear implant users. Spatial masking patterns and the measures of place specificity were similar between forward and interleaved masking. Unlike acoustic hearing where broader tuning curves are obtained in simultaneous masking, the type of masking experiment did not influence the measure of place specificity in cochlear implants.

Place specificity of monopolar and tripolar stimuli in cochlear implants: the influence of residual masking.

This experiment investigated whether place specificity of neural activity evoked by cochlear implant stimulation is improved in tripolar compared to monopolar mode using a forward masking protocol addressing some limitations of previous methods of measurement and analysis. The amount of residual masking (masking remaining at long masker-probe delays) was also measured, and its potential influence on the specificity measures was evaluated. The masker stimulus comprised equally loud interleaved mono- or tripolar stimulation on two electrodes equidistant from a central probe electrode in an apical and basal direction, reducing the influence of off-site listening. The effect of masker-probe distance on the threshold shift of the tripolar probe was analyzed to derive a measure of place specificity. On average, tripolar maskers were more place specific than monopolar maskers, although the mean effect was small. There was no significant effect of masker level on specificity or on the differences observed between modes. The mean influence of residual masking on normalized masking functions was similar for the two modes and, therefore, did not influence the comparison of specificity between the modes. However, variability in amount of residual masking was observed between subjects, and therefore should be considered in forward masking studies that compare place specificity across subjects.

Connections between spatially distant primary language regions strengthen with age during infancy, as revealed by resting-state fNIRS.

Objective.Hearing is an important sensory function that plays a key role in how children learn to speak and develop language skills. Although previous neuroimaging studies have established that much of brain network maturation happens in early childhood, our understanding of the developmental trajectory of language areas is still very limited. We hypothesized that typical development trajectory of language areas in early childhood could be established by analyzing the changes of functional connectivity in normal hearing infants at different ages using functional near-infrared spectroscopy.Approach.Resting-state data were recorded from two bilateral temporal and prefrontal regions associated with language processing by measuring the relative changes of oxy-hemoglobin (HbO) and deoxy-hemoglobin (HbR) concentrations. Connectivity was calculated using magnitude-squared coherence of channel pairs located in (a) inter-hemispheric homologous and (b) intra-hemispheric brain regions to assess connectivity between homologous regions across hemispheres and two regions of interest in the same hemisphere, respectively.Main results.A linear regression model fitted to the age vs coherence of inter-hemispheric homologous test group revealed a significant coefficient of determination for both HbO (R2= 0.216,p= 0.0169) and HbR (R2= 0.206,p= 0.0198). A significant coefficient of determination was also found for intra-hemispheric test group for HbO (R2= 0.237,p= 0.0117) but not for HbR (R2= 0.111,p= 0.0956).Significance.The findings from HbO data suggest that both inter-hemispheric homologous and intra-hemispheric connectivity between primary language regions significantly strengthen with age in the first year of life. Mapping out the developmental trajectory of primary language areas of normal hearing infants as measured by functional connectivity could potentially allow us to better understand the altered connectivity and its effects on language delays in infants with hearing impairments.

Investigating the Effect of Data Length on the Performance of Frequency-Domain fNIRS Functional Connectivity Measures.

Resting-state functional connectivity is a promising tool for understanding and characterizing brain network architecture. However, obtaining uninterrupted long recording of resting-state data is challenging in many clinically relevant populations. Moreover, the interpretation of connectivity results may heavily depend on the data length and functional connectivity measure used. We compared the performance of three frequency-domain connectivity measures: magnitude-squared, wavelet and multitaper coherence; and the effect of data length ranging from 3 to 9 minutes. Performance was characterized by distinguishing two groups of channel pairs with known different connectivity strengths. While all methods considered improved the ability to distinguish the two groups with increasing data lengths, wavelet coherence performed best for the shortest time window of 3 minutes. Knowledge of which measure is more reliably used when shorter fNIRS recordings are available could make the utility of functional connectivity biomarkers more feasible in clinical populations of interest.

Brain Functional Connectivity Networks do not Return to Resting-state During Control Trials in Block Design Experiments.

Many studies on morphology analysis show that if short inter-stimulus intervals separate tasks, the hemodynamic response amplitude will return to the resting-state baseline before the subsequent stimulation onset; hence, responses to successive tasks do not overlap. Accordingly, popular brain imaging analysis techniques assume changes in hemodynamic response amplitude subside after a short time (around 15 seconds). However, whether this assumption holds when studying brain functional connectivity has yet to be investigated. This paper assesses whether or not the functional connectivity network in control trials returns to the resting-state functional connectivity network. Traditionally, control trials in block-design experiments are used to evaluate response morphology to no stimulus. We analyzed data from an event-related experiment with audio and visual stimuli and resting state. Our results showed that functional connectivity networks during control trials were more similar to that of tasks than resting-state networks. In other words, contrary to task-related changes in the hemodynamic amplitude, where responses settle after a short time, the brain's functional connectivity networks do not return to their intrinsic resting-state network in such short intervals.