Frequency-following Response Research Articles

Concussion acutely disrupts auditory processing in division I football student-athletes

ABSTRACT Introduction Diagnosis, assessment, and management of sports-related concussion require a multi-modal approach. Yet, currently, an objective assessment of auditory processing is not included. The auditory system is uniquely complex, relying on exquisite temporal precision to integrate signals across many synapses, connected by long axons. Given this complexity and precision, together with the fact that axons are highly susceptible to damage from mechanical force, we hypothesize that auditory processing is susceptible to concussive injury. Methods We measured the frequency-following response (FFR), a scalp-recorded evoked potential that assesses processing of complex sound features, including pitch and phonetic identity. FFRs were obtained on male Division I Collegiate football players prior to contact practice to determine a pre-season baseline of auditory processing abilities, and again after sustaining a sports-related concussion. We predicted that concussion would decrease pitch and phonetic processing relative to the student-athlete’s preseason baseline. Results We found that pitch and phonetic encoding was smaller post-concussion. Student-athletes who sustained a second concussion showed similar declines after each injury. Conclusions Auditory processing should be included in the multimodal assessment of sports-related concussion. Future studies that extend this work to other sports, other injuries (e.g. blast exposure), and to female athletes are needed.

Musical training does not enhance neural sound encoding at early stages of the auditory system: A large-scale multisite investigation.

Musical training has been associated with enhanced neural processing of sounds, as measured via the frequency following response (FFR), implying the potential for human subcortical neural plasticity. We conducted a large-scale multi-site preregistered study (n > 260) to replicate and extend the findings underpinning this important relationship. We failed to replicate any of the major findings published previously in smaller studies. Musical training was related neither to enhanced spectral encoding strength of a speech stimulus (/da/) in babble nor to a stronger neural-stimulus correlation. Similarly, the strength of neural tracking of a speech sound with a time-varying pitch was not related to either years of musical training or age of onset of musical training. Our findings provide no evidence for plasticity of early auditory responses based on musical training and exposure.

Individual differences in the consistency of neural and behavioural responses to speech sounds

There are documented individual differences among adults in the consistency of speech sound processing, both at neural and behavioural levels. Some adults show more consistent neural responses to speech sounds than others, as measured by an event-related potential called the frequency-following response (FFR); similarly, some adults show more consistent behavioural responses to native speech sounds than others, as measured by two-alternative forced choice (2AFC) and visual analog scaling (VAS) tasks. Adults also differ in how successfully they can perceive non-native speech sounds. Interestingly, it remains unclear whether these differences are related within individuals. In the current study, native English-speaking adults completed native phonetic perception tasks (2AFC and VAS), a non-native (German) phonetic perception task, and an FFR recording session. From these tasks, we derived measures of the consistency of participants’ neural and behavioural responses to native speech as well as their non-native perception ability. We then examined the relationships among individual differences in these measures. Analysis of the behavioural measures revealed that more consistent responses to native sounds predicted more successful perception of unfamiliar German sounds. Analysis of neural and behavioural data did not reveal clear relationships between FFR consistency and our phonetic perception measures. This multimodal work furthers our understanding of individual differences in speech processing among adults, and may eventually lead to individualized approaches for enhancing non-native language acquisition in adulthood.

No Evidence of Musical Training Influencing the Cortical Contribution to the Speech-Frequency-Following Response and Its Modulation through Selective Attention.

Musicians can have better abilities to understand speech in adverse condition such as background noise than non-musicians. However, the neural mechanisms behind such enhanced behavioral performances remain largely unclear. Studies have found that the subcortical frequency-following response to the fundamental frequency of speech and its higher harmonics (speech-FFR) may be involved since it is larger in people with musical training than in those without. Recent research has shown that the speech-FFR consists of a cortical contribution in addition to the subcortical sources. Both the subcortical and the cortical contribution are modulated by selective attention to one of two competing speakers. However, it is unknown whether the strength of the cortical contribution to the speech-FFR, or its attention modulation, is influenced by musical training. Here we investigate these issues through magnetoencephalographic (MEG) recordings of 52 subjects (18 musicians, 25 non-musicians, and 9 neutral participants) listening to two competing male speakers while selectively attending one of them. The speech-in-noise comprehension abilities of the participants were not assessed. We find that musicians and non-musicians display comparable cortical speech-FFRs and additionally exhibit similar subject-to-subject variability in the response. Furthermore, we also do not observe a difference in the modulation of the neural response through selective attention between musicians and non-musicians. Moreover, when assessing whether the cortical speech-FFRs are influenced by particular aspects of musical training, no significant effects emerged. Taken together, we did not find any effect of musical training on the cortical speech-FFR.

Machine Learning Recognizes Frequency-Following Responses in American Adults: Effects of Reference Spectrogram and Stimulus Token.

Electrophysiological research has been widely utilized to study brain responses to acoustic stimuli. The frequency-following response (FFR), a non-invasive reflection of how the brain encodes acoustic stimuli, is a particularly propitious electrophysiologic measure. While the FFR has been studied extensively, there are limitations in obtaining and analyzing FFR recordings that recent machine learning algorithms may address. In this study, we aimed to investigate whether FFRs can be enhanced using an "improved" source-separation machine learning algorithm. For this study, we recruited 28 native speakers of American English with normal hearing. We obtained two separate FFRs from each participant while they listened to two stimulus tokens /i/ and /da/. Electroencephalographic signals were pre-processed and analyzed using a source-separation non-negative matrix factorization (SSNMF) machine learning algorithm. The algorithm was trained using individual, grand-averaged, or stimulus token spectrograms as a reference. A repeated measures analysis of variance revealed that FFRs were significantly enhanced (p < .001) when the "improved" SSNMF algorithm was trained using both individual and grand-averaged spectrograms, but not when utilizing the stimulus token spectrogram. Similar results were observed when extracting FFRs elicited by using either stimulus token, /i/ or /da/. This demonstration shows how the SSNMF machine learning algorithm, using individual and grand-averaged spectrograms as references in training the algorithm, significantly enhanced FFRs. This improvement has important implications for the obtainment and analytical processes of FFR, which may lead to advancements in clinical applications of FFR testing.

Inhibitory effects of prepulse stimuli on the electrophysiological responses to startle stimuli in the deep layers of the superior colliculus.

Prepulse inhibition (PPI) is a phenomenon where a weak prepulse stimulus inhibits the startle reflex to a subsequent stronger stimulus, which can be induced by various sensory stimulus modalities such as visual, tactile, and auditory stimuli. This study investigates the neural mechanisms underlying auditory PPI by focusing on the deep layers of the superior colliculus (deepSC) and the inferior colliculus (IC) in rats. Nineteen male Sprague-Dawley rats were implanted with electrodes in the left deepSC and the right IC, and electrophysiological recordings were conducted under anesthesia to observe the frequency following responses (FFRs) to startle stimuli with and without prepulse stimuli. Our results showed that in the deepSC, narrowband noise as a prepulse stimulus significantly inhibited the envelope component of the startle response, while the fine structure component remained unaffected. However, this inhibitory effect was not observed in the IC or when the prepulse stimulus was a gap. These findings suggest that the deepSC plays a crucial role in the neural circuitry of PPI, particularly in the modulation of the envelope component of the startle response. The differential effects of narrowband noise and gap as prepulse stimuli also indicate distinct neural pathways for sound-induced PPI and Gap-PPI. Understanding these mechanisms could provide insights into sensory processing and potential therapeutic targets for disorders involving impaired PPI, such as tinnitus.

Voice actors show enhanced neural tracking of pitch, prosody perception, and music perception

Experiences with sound that make strong demands on the precision of perception, such as musical training and experience speaking a tone language, can enhance auditory neural encoding. Are high demands on the precision of perception necessary for training to drive auditory neural plasticity? Voice actors are an ideal subject population for answering this question. Voice acting requires exaggerating prosodic cues to convey emotion, character, and linguistic structure, drawing upon attention to sound, memory for sound features, and accurate sound production, but not fine perceptual precision. Here we assessed neural encoding of pitch using the frequency-following response (FFR), as well as prosody, music, and sound perception, in voice actors and a matched group of non-actors. We find that the consistency of neural sound encoding, prosody perception, and musical phrase perception are all enhanced in voice actors, suggesting that a range of neural and behavioural auditory processing enhancements can result from training which lacks fine perceptual precision. However, fine discrimination was not enhanced in voice actors but was linked to degree of musical experience, suggesting that low-level auditory processing can only be enhanced by demanding perceptual training. These findings suggest that training which taxes attention, memory, and production but is not perceptually taxing may be a way to boost neural encoding of sound and auditory pattern detection in individuals with poor auditory skills.

Myogenic artifacts masquerade as neuroplasticity in the auditory frequency-following response.

The frequency-following response (FFR) is an evoked potential that provides a neural index of complex sound encoding in the brain. FFRs have been widely used to characterize speech and music processing, experience-dependent neuroplasticity (e.g., learning and musicianship), and biomarkers for hearing and language-based disorders that distort receptive communication abilities. It is widely assumed that FFRs stem from a mixture of phase-locked neurogenic activity from the brainstem and cortical structures along the hearing neuraxis. In this study, we challenge this prevailing view by demonstrating that upwards of ~50% of the FFR can originate from an unexpected myogenic source: contamination from the postauricular muscle (PAM) vestigial startle reflex. We measured PAM, transient auditory brainstem responses (ABRs), and sustained frequency-following response (FFR) potentials reflecting myogenic (PAM) and neurogenic (ABR/FFR) responses in young, normal-hearing listeners with varying degrees of musical training. We first establish that PAM artifact is present in all ears, varies with electrode proximity to the muscle, and can be experimentally manipulated by directing listeners' eye gaze toward the ear of sound stimulation. We then show this muscular noise easily confounds auditory FFRs, spuriously amplifying responses 3-4-fold with tandem PAM contraction and even explaining putative FFR enhancements observed in highly skilled musicians. Our findings expose a new and unrecognized myogenic source to the FFR that drives its large inter-subject variability and cast doubt on whether changes in the response typically attributed to neuroplasticity/pathology are solely of brain origin.

Neural Delays in Processing Speech in Background Noise Minimized after Short-Term Auditory Training.

Background noise disrupts the neural processing of sound, resulting in delayed and diminished far-field auditory-evoked responses. In young adults, we previously provided evidence that cognitively based short-term auditory training can ameliorate the impact of background noise on the frequency-following response (FFR), leading to greater neural synchrony to the speech fundamental frequency(F0) in noisy listening conditions. In this same dataset (55 healthy young adults), we now examine whether training-related changes extend to the latency of the FFR, with the prediction of faster neural timing after training. FFRs were measured on two days separated by ~8 weeks. FFRs were elicited by the syllable "da" presented at a signal-to-noise ratio (SNR) of +10 dB SPL relative to a background of multi-talker noise. Half of the participants participated in 20 sessions of computerized training (Listening and Communication Enhancement Program, LACE) between test sessions, while the other half served as Controls. In both groups, half of the participants were non-native speakers of English. In the Control Group, response latencies were unchanged at retest, but for the training group, response latencies were earlier. Findings suggest that auditory training can improve how the adult nervous system responds in noisy listening conditions, as demonstrated by decreased response latencies.

Binaural responses to a speech syllable are altered in children with hearing loss: Evidence from the frequency-following response

Background & rationaleIn prior work using non-speech stimuli, children with hearing loss show impaired perception of binaural cues and no significant change in cortical responses to bilateral versus unilateral stimulation. Aims of the present study were to: 1) identify bilateral responses to envelope and spectral components of a speech syllable using the frequency-following response (FFR), 2) determine if abnormalities in the bilateral FFR occur in children with hearing loss, and 3) assess functional consequences of abnormal bilateral FFR responses on perception of binaural timing cues. MethodsA single-syllable speech stimulus (/dα/) was presented to each ear individually and bilaterally. Participants were 9 children with normal hearing (MAge = 12.1 ± 2.5 years) and 6 children with bilateral hearing loss who were experienced bilateral hearing aid users (MAge = 14.0 ± 2.6 years). FFR temporal and spectral peak amplitudes were compared between listening conditions and groups using linear mixed model regression analyses. Behavioral sensitivity to binaural cues were measured by lateralization responses as coming from the right or left side of the head. ResultsBoth temporal and spectral peaks in FFR responses increased in amplitude in the bilateral compared to unilateral listening conditions in children with normal hearing. These measures of “bilateral advantage” were reduced in the group of children with bilateral hearing loss and associated with decreased sensitivity to interaural timing differences. ConclusionThis study is the first to show that bilateral responses in both temporal and spectral domains can be measured in children using the FFR and is altered in children with hearing loss with consequences to binaural hearing.

Exposure to bilingual or monolingual maternal speech during pregnancy affects the neurophysiological encoding of speech sounds in neonates differently.

Exposure to maternal speech during the prenatal period shapes speech perception and linguistic preferences, allowing neonates to recognize stories heard frequently in utero and demonstrating an enhanced preference for their mother's voice and native language. Yet, with a high prevalence of bilingualism worldwide, it remains an open question whether monolingual or bilingual maternal speech during pregnancy influence differently the fetus' neural mechanisms underlying speech sound encoding. In the present study, the frequency-following response (FFR), an auditory evoked potential that reflects the complex spectrotemporal dynamics of speech sounds, was recorded to a two-vowel /oa/ stimulus in a sample of 129 healthy term neonates within 1 to 3 days after birth. Newborns were divided into two groups according to maternal language usage during the last trimester of gestation (monolingual; bilingual). Spectral amplitudes and spectral signal-to-noise ratios (SNR) at the stimulus fundamental (F0) and first formant (F1) frequencies of each vowel were, respectively, taken as measures of pitch and formant structure neural encoding. Our results reveal that while spectral amplitudes at F0 did not differ between groups, neonates from bilingual mothers exhibited a lower spectral SNR. Additionally, monolingually exposed neonates exhibited a higher spectral amplitude and SNR at F1 frequencies. We interpret our results under the consideration that bilingual maternal speech, as compared to monolingual, is characterized by a greater complexity in the speech sound signal, rendering newborns from bilingual mothers more sensitive to a wider range of speech frequencies without generating a particularly strong response at any of them. Our results contribute to an expanding body of research indicating the influence of prenatal experiences on language acquisition and underscore the necessity of including prenatal language exposure in developmental studies on language acquisition, a variable often overlooked yet capable of influencing research outcomes.

The frequency-following response in late preterm neonates: a pilot study.

Infants born very early preterm are at high risk of language delays. However, less is known about the consequences of late prematurity. Hence, the aim of the present study is to characterize the neural encoding of speech sounds in late preterm neonates in comparison with those born at term. The speech-evoked frequency-following response (FFR) was recorded to a consonant-vowel stimulus /da/ in 36 neonates in three different groups: 12 preterm neonates [mean gestational age (GA) 36.05 weeks], 12 "early term neonates" (mean GA 38.3 weeks), and "late term neonates" (mean GA 41.01 weeks). From the FFR recordings, a delayed neural response and a weaker stimulus F0 encoding in premature neonates compared to neonates born at term was observed. No differences in the response time onset nor in stimulus F0 encoding were observed between the two groups of neonates born at term. No differences between the three groups were observed in the neural encoding of the stimulus temporal fine structure. These results highlight alterations in the neural encoding of speech sounds related to prematurity, which were present for the stimulus F0 but not for its temporal fine structure.

Artifact removal by template subtraction enables recordings of the frequency following response in cochlear-implant users

Electrically evoked frequency-following responses (eFFRs) provide insight in the phase-locking ability of brainstem of cochlear-implant (CI) users. eFFRs can potentially be used to gain insight in the individual differences in the biological limitation on temporal encoding of the electrically stimulated auditory pathway, which can be inherent to the electrical stimulation itself and/or the degenerative processes associated with hearing loss. One of the major challenge of measuring eFFRs in CI users is the process of isolating the stimulation artifact from the neural response, as both the response and the artifact overlap in time and have similar frequency characteristics. Here we introduce a new artifact removal method based on template subtraction that successfully removes the stimulation artifacts from the recordings when CI users are stimulated with pulse trains from 128 to 300 pulses per second in a monopolar configuration. Our results show that, although artifact removal was successful in all CI users, the phase-locking ability of the brainstem to the different pulse rates, as assessed with the eFFR differed substantially across participants. These results show that the eFFR can be measured, free from artifacts, in CI users and that they can be used to gain insight in individual differences in temporal processing of the electrically stimulated auditory pathway.

Feel sounds with your hands: Exploring tactile frequency-following response

Auditory perception is often influence by other senses. Prior studies have documented that the auditory cortex can respond to vibration, but the nature of this neural response remains unclear. The frequency-following response (FFR) is a non-invasive evoked brain response that can be used to study the fidelity of periodicity encoding of complex sounds. The main goal of this study was to investigate if tactile processing of sounds retains periodicity information as measured by the FFR. We acquired electroencephalography while participants were presented with repetitions of a synthesized speech syllable /da/ under three conditions (Auditory, Tactile, and both). A technology developed within our laboratory (Multichannel Vibrotactile Glove) was used to present sounds to all fingers. Results reveal that it is possible to measure a tactile FFR using vibrotactile stimulation, which is similar to the auditory FFR, but exhibits somewhat different characteristics as compared to unimodal auditory FFR, including lower amplitude and no sensitivity to harmonics. These findings suggest that these modalities interact, opening up questions about the origins and pathways responsible for the phenomena and introduces potential uses of tactile perception to mitigate the effect of hearing loss in speech and music perception.

Predicting early auditory evoked potentials using a computational model of auditory-nerve processing.

Non-invasive electrophysiological measures, such as auditory evoked potentials (AEPs), play a crucial role in diagnosing auditory pathology. However, the relationship between AEP morphology and cochlear degeneration remains complex and not well understood. Dau [J. Acoust. Soc. Am. 113, 936-950 (2003)] proposed a computational framework for modeling AEPs that utilized a nonlinear auditory-nerve (AN) model followed by a linear unitary response function. While the model captured some important features of the measured AEPs, it also exhibited several discrepancies in response patterns compared to the actual measurements. In this study, an enhanced AEP modeling framework is presented, incorporating an improved AN model, and the conclusions from the original study were reevaluated. Simulation results with transient and sustained stimuli demonstrated accurate auditory brainstem responses (ABRs) and frequency-following responses (FFRs) as a function of stimulation level, although wave-V latencies remained too short, similar to the original study. When compared to physiological responses in animals, the revised model framework showed a more accurate balance between the contributions of auditory-nerve fibers (ANFs) at on- and off-frequency regions to the predicted FFRs. These findings emphasize the importance of cochlear processing in brainstem potentials. This framework may provide a valuable tool for assessing human AN models and simulating AEPs for various subtypes of peripheral pathologies, offering opportunities for research and clinical applications.

The Early Subcortical Response at the Fundamental Frequency of Speech Is Temporally Separated from Later Cortical Contributions.

Most parts of speech are voiced, exhibiting a degree of periodicity with a fundamental frequency and many higher harmonics. Some neural populations respond to this temporal fine structure, in particular at the fundamental frequency. This frequency-following response to speech consists of both subcortical and cortical contributions and can be measured through EEG as well as through magnetoencephalography (MEG), although both differ in the aspects of neural activity that they capture: EEG is sensitive to both radial and tangential sources as well as to deep sources, whereas MEG is more restrained to the measurement of tangential and superficial neural activity. EEG responses to continuous speech have shown an early subcortical contribution, at a latency of around 9 msec, in agreement with MEG measurements in response to short speech tokens, whereas MEG responses to continuous speech have not yet revealed such an early component. Here, we analyze MEG responses to long segments of continuous speech. We find an early subcortical response at latencies of 4-11 msec, followed by later right-lateralized cortical activities at delays of 20-58 msec as well as potential subcortical activities. Our results show that the early subcortical component of the FFR to continuous speech can be measured from MEG in populations of participants and that its latency agrees with that measured with EEG. They furthermore show that the early subcortical component is temporally well separated from later cortical contributions, enabling an independent assessment of both components toward further aspects of speech processing.

Short- and long-term neuroplasticity interact during the perceptual learning of concurrent speech.

Plasticity from auditory experience shapes the brain's encoding and perception of sound. However, whether such long-term plasticity alters the trajectory of short-term plasticity during speech processing has yet to be investigated. Here, we explored the neural mechanisms and interplay between short- and long-term neuroplasticity for rapid auditory perceptual learning of concurrent speech sounds in young, normal-hearing musicians and nonmusicians. Participants learned to identify double-vowel mixtures during ~ 45min training sessions recorded simultaneously with high-density electroencephalography (EEG). We analyzed frequency-following responses (FFRs) and event-related potentials (ERPs) to investigate neural correlates of learning at subcortical and cortical levels, respectively. Although both groups showed rapid perceptual learning, musicians showed faster behavioral decisions than nonmusicians overall. Learning-related changes were not apparent in brainstem FFRs. However, plasticity was highly evident in cortex, where ERPs revealed unique hemispheric asymmetries between groups suggestive of different neural strategies (musicians: right hemisphere bias; nonmusicians: left hemisphere). Source reconstruction and the early (150-200ms) time course of these effects localized learning-induced cortical plasticity to auditory-sensory brain areas. Our findings reinforce the domain-general benefits of musicianship but reveal that successful speech sound learning is driven by a critical interplay between long- and short-term mechanisms of auditory plasticity, which first emerge at a cortical level.

Encoding of speech sounds with frequency-following response in infants with Congenital Zika Syndrome: A case-controlled study

Encoding of speech sounds with frequency-following response in infants with Congenital Zika Syndrome: A case-controlled study

Advancing Auditory Processing by Detecting Frequency-Following Responses Through a Specialized Machine Learning Model.

In this study, we explore the feasibility and performance of detecting scalp-recorded frequency-following responses (FFRs) with a specialized machine learning (ML) model. By leveraging the strengths of feature extraction of the source separation non-negative matrix factorization (SSNMF) algorithm and its adeptness in handling limited training data, we adapted the SSNMF algorithm into a specialized ML model with a hybrid architecture to enhance FFR detection amidst background noise. We recruited 40 adults with normal hearing and evoked their scalp recorded FFRs using the English vowel/i/with a rising pitch contour. The model was trained on FFR-present and FFR-absent conditions, and its performance was evaluated using sensitivity, specificity, efficiency, false-positive rate, and false-negative rate metrics. This study revealed that the specialized SSNMF model achieved heightened sensitivity, specificity, and efficiency in detecting FFRs as the number of recording sweeps increased. Sensitivity exceeded 80% at 500 sweeps and maintained over 89% from 1000 sweeps onwards. Similarly, specificity and efficiency also improved rapidly with increasing sweeps. The progressively enhanced sensitivity, specificity, and efficiency of this specialized ML model underscore its practicality and potential for broader applications. These findings have immediate implications for FFR research and clinical use, while paving the way for further advancements in the assessment of auditory processing.

Subcortical Auditory Processing and Speech Perception in Noise Among Individuals With and Without Extended High-Frequency Hearing Loss.

The significance of extended high-frequency (EHF) hearing (> 8 kHz) is not well understood so far. In this study, we aimed to understand the relationship between EHF hearing loss (EHFHL) and speech perception in noise (SPIN) and the associated physiological signatures using the speech-evoked frequency-following response (sFFR). Sixteen young adults with EHFHL and 16 age- and sex-matched individuals with normal hearing participated in the study. SPIN performance in right speech-right noise, left speech-left noise, and binaural listening conditions was evaluated using the Turkish Matrix Test. Additionally, subcortical auditory processing was assessed by recording sFFRs elicited by 40-ms /da/ stimuli. Individuals with EHFHL demonstrated poorer SPIN performances in all listening conditions (p < .01). Longer latencies were observed in the V (onset) and O (offset) peaks in these individuals (p ≤ .01). However, only the V/A peak amplitude was found to be significantly reduced in individuals with EHFHL (p < .01). Our findings highlight the importance of EHF hearing and suggest that EHF hearing should be considered among the key elements in SPIN. Individuals with EHFHL show a tendency toward weaker subcortical auditory processing, which likely contributes to their poorer SPIN performance. Thus, routine assessment of EHF hearing should be implemented in clinical settings, alongside the evaluation of standard audiometric frequencies (0.25-8 kHz).