Human frequency-following responses to monaural and binaural stimuli

doi:10.1016/0013-4694(75)90262-X

Electroencephalography and Clinical Neurophysiology

Volume 38, Issue 4, April 1975, Pages 379-386

https://doi.org/10.1016/0013-4694(75)90262-X Get rights and content

Abstract

Frequency-following responses, with latencies circa 6 msec, were recorded from five normal-hearing human subjects to brief 500 c/sec tone bursts presented monaurally. The frequency-following responses appear as peaks occurring at 2 msec intervals superimposed on a slow wave (pedestal-like) component. Comparisons were made between the frequency-following responses evoked by binaural and monaural stimuli. The results show that the binaural responses may be interpreted as the sum of two monaural responses. It is concluded, therefore, that there are two independent populations of neurons, each capable of generating a frequency-following response and each activated by one ear. It is also argued that the frequency-following response is not a microphonic-like response but rather that the individual waves in the frequency-following response are evoked by the collective activity of phase-locked single units. Finally, on the basis of the distinctness of the individual waves in the frequency-following response, it is concluded that the neural generators of the response must be spatially compact.

Résumé

Des réponses en fonction de la fréquence des stimulus dont les latences sont autour de 6 msec ont été enregistrées chez 5 sujets avec audition normale, à des bouffées de sons brefs de 500 c/sec présentés de façon mono-auriculaire. Les réponses en fonction de la fréquence du stimulus s'observent sous forme de pics survenant à des intervalles de 2 msec, surimposés à une composante lente (semblable à un palier). Des comparaisons ont été réalisées entre les réponses évoquées à des stimuli mono et bi-auriculaires. Les résultats montrent que les réponses bi-auriculaires peuvent être interprétées comme la somme des deux réponses mono-auriculaires. Les auteurs concluent ainsi qu'il y a deux populations indépendantes de neurones, chacune d'entre elles étant capable d'engendrer une réponse en fonction de la fréquence du stimulus et d'être activée par une oreille. Il est également souligné que les réponses ne sont de type microphonique mais plutôt que les ondes individuelles qui les constituent sont évoquées par l'activité collective de cellules unitaires en phase. Enfin, sur la base de la distinction des ondes individuelles dans la réponse, les auteurs concluent que les générateurs neuroniques de cette réponse doivent être spatialement très groupés.

References (10)

J.L. Martin et al.
Short-latency auditory evoked responses recorded from human nasopharynx
Brain Res.
(1973)
G. Moushegian et al.
Neuronal response correlates of cochlear nucleus: evidence for restrictive and multiple parameter information transfer
Exp. Neurol.
(1970)
G. Moushegian et al.
Scalp-recorded early responses in man to frequencies in the speech range
Electroenceph. clin. Neurophysiol.
(1973)
T.W. Picton et al.
Human auditory evoked potentials. I. Evaluation of components
Electroenceph. clin. Neurophysiol.
(1974)
D.L. Jewett et al.
Auditory-evoked far fields averaged from the scalp of humans
Brain
(1971)

There are more references available in the full text version of this article.

Cited by (57)

Methodological considerations when measuring and analyzing auditory steady-state responses with multi-channel EEG
2022, Current Research in Neurobiology
The auditory steady-state response (ASSR) has been traditionally recorded with few electrodes and is often measured as the voltage difference between mastoid and vertex electrodes (vertical montage). As high-density EEG recording systems have gained popularity, multi-channel analysis methods have been developed to integrate the ASSR signal across channels. The phases of ASSR across electrodes can be affected by factors including the stimulus modulation rate and re-referencing strategy, which will in turn affect the estimated ASSR strength. To explore the relationship between the classical vertical-montage ASSR and whole-scalp ASSR, we applied these two techniques to the same data to estimate the strength of ASSRs evoked by tones with sinusoidal amplitude modulation rates of around 40, 100, and 200 Hz. The whole-scalp methods evaluated in our study, with either linked-mastoid or common-average reference, included ones that assume equal phase across all channels, as well as ones that allow for different phase relationships. The performance of simple averaging was compared to that of more complex methods involving principal component analysis. Overall, the root-mean-square of the phase locking values (PLVs) across all channels provided the most efficient method to detect ASSR across the range of modulation rates tested here.
Dichotic phase effects on frequency following responses reveal phase variant and invariant harmonic distortion products
2019, Hearing Research
Citation Excerpt :
This suggests that the placement of the electrodes might be a crucial factor in studying the binaural processing using FFRs. Thus, the varied results in binaural FFRs in literature could at least in part be attributed to the electrode placement at the vertex (Ballachanda and Moushegian, 2000; Gerken et al., 1975; Uppunda et al., 2015) vs. the forehead (Clark et al., 1997; Krishnan and McDaniel, 1998; Wilson and Krishnan, 2005). Shinn-Cunningham et al. (2017) suggest that the binaural envelope following responses to click trains do not have enough evidence for binaural processing component.
The dichotic frequency following responses (FFR) have been used in studies to infer about dichotic auditory processing. In the present study, we hypothesize that the proximity of the binaural neural generators of the FFR would result in interference of the volume-conducted electrical fields. This might lead to contamination of the scalp-recorded dichotic FFRs due to which it might be difficult to infer about true dichotic processing in the putative neural generators. We investigated this by recording FFRs to binaurally presented 200 Hz pure tone with graded dichotic phase offsets (0°, 90°, 180° and 270°) in normal hearing young adults. Spectral analysis of the FFRs was performed for the estimation of the magnitude and phase at the component frequencies. FFR spectra were compared using non-parametric paired randomizations within the subjects. We found that the brainstem responses to a 200 Hz pure tone consisted of prominent peaks at 200 Hz, and at frequencies corresponding to the harmonics of 200 Hz. The FFR spectral magnitude at 200 Hz diminished with a phase offset of 180°. Phase offsets of 90° and 270° showed reduced spectral magnitudes at 200 Hz than those in the 0° condition. Our findings, in line with the hypothesis, show that the dichotic FFRs do not reflect true dichotic processing and that they are contaminated during volume conduction. Additionally, we found harmonic distortion products (HDP) in the FFRs. We found that the response at 200 Hz and the 3rd HDP systematically varied with a change in phase of the stimulus, while the even HDPs (2nd and 4th) were phase-invariant. Based on our findings, and modeling FFRs using auditory models, we propose a rectification process as the contributors for the generation of HDPs. We also discuss the implications of this HDP generating mechanism in understanding the pitch represented in FFRs.
Differences between auditory frequency-following responses and onset responses: Intracranial evidence from rat inferior colliculus
2018, Hearing Research
Citation Excerpt :
As mentioned in the Introduction, neurons with the onset-firing pattern and those with the sustained firing pattern are two of the major neuron types in the ICC (Wagner, 1994; Li and Kelly, 1992a,b, 1998; Reetz and Ehret, 1999; Peruzzi et al., 2000; Sivaramakrishnan and Oliver, 2001; Bal et al., 2002). There has been a long debate regarding whether sustained FFRs are based on overlapping transient auditory brainstem evoked potentials (e.g., Daly et al., 1976; Dau, 2003; Davis and Hirsh, 1974; Gerken et al., 1975; Picton et al., 1978, Goldstein and Kiang, 1958; Janssen et al., 1991; Bidelman, 2015). Both the present studies with animal intracranial recordings and some previous studies with human scalp EEG recordings (e.g., Bidelman, 2015) have suggested that the sustained phase-locked FFRs and onset responses in the IC are auditory brain responses with separated underlying neural mechanisms.
A periodic sound, such as a pure tone, evokes both transient onset field-potential responses and sustained frequency-following responses (FFRs) in the auditory midbrain, the inferior colliculus (IC). It is not clear whether the two types of responses are based on the same or different neural substrates. Although it has been assumed that FFRs are based on phase locking to the periodic sound, the evidence showing the direct relationship between the FFR amplitude and the phase-locking strength is still lacking. Using intracranial recordings from the rat central nucleus of inferior colliculus (ICC), this study was to examine whether FFRs and onset responses are different in sensitivity to pure-tone frequency and/or response-stimulus correlation, when a tone stimulus is presented either monaurally or binaurally. Particularly, this study was to examine whether the FFR amplitude is correlated with the strength of phase locking. The results showed that with the increase of tone-stimulus frequency from 1 to 2 kHz, the FFR amplitude decreased but the onset-response amplitude increased. Moreover, the FFR amplitude, but not the onset-response amplitude, was significantly correlated with the phase coherence between tone-evoked potentials and the tone stimulus. Finally, the FFR amplitude was negatively correlated with the onset-response amplitude. These results indicate that periodic-sound-evoked FFRs are based on phase-locking activities of sustained-response neurons, but onset responses are based on transient activities of onset-response neurons, suggesting that FFRs and onset responses are associated with different functions.
Multichannel recordings of the human brainstem frequency-following response: Scalp topography, source generators, and distinctions from the transient ABR
2015, Hearing Research
Citation Excerpt :
Under the stimuli used here (i.e., periodic click trains), the convolution of the ABR as an explanation for the FFR represents somewhat of a special (extreme) case but offers the best possible chance of observing convergence between the two responses. Yet, our data suggest that this “convolution model” of FFR generation is not an accurate description for the sustained response (cf. Davis and Hirsh, 1974; Gerken et al., 1975; Janssen et al., 1991). For all F0s tested, FFRs derived from individual's repeated ABR showed multiple dissociations in both spectral and temporal features.
Brainstem frequency-following responses (FFRs) probe the neural transcription of speech/music, auditory disorders, and plasticity in subcortical auditory function. Despite clinical and empirical interest, the response's neural basis remains poorly understood. The current study aimed to more fully characterize functional properties of the human FFR (topography, source locations, generation). Speech-evoked FFRs were recorded using a high-density (64 channel) electrode montage. Source dipole modeling and 3-channel Lissajous analysis was used to localize the most likely FFR generators and their orientation trajectories. Additionally, transient auditory brainstem responses (ABRs), recorded in the same listeners, were used to predict FFRs and test the long-held assumption that the sustained potential reflects a series of overlapping onset responses. Results showed that FFRs were maximal at frontocentral scalp locations with obliquely oriented sources from putative generators in the midbrain (i.e., upper brainstem). Comparisons between derived and actual recordings revealed the FFR is not a series of repeated ABR wavelets and thus, represents a functionally distinct brainstem response. FFRs recorded at temporal electrode sites showed larger amplitudes and contained higher frequency components than vertex channels (Fz, Cz) suggesting that FFRs measured near the mastoid are generated more peripherally (auditory nerve) than measurements at frontocentral scalp locations. Furthermore, this reveals the importance of choice in reference electrode location for FFR interpretation. Our findings provide non-invasive evidence that (i) FFRs reflect sustained neural activity whose sources are consistent with rostral brainstem generators and (ii) FFRs are functionally distinct from the onset ABR response.
Exploration of the auditory system in humans: From click to speech auditory brainstem responses
2010, Neurophysiologie Clinique
La compréhension et l’évaluation des soubassements neurophysiologiques de la perception de la parole au niveau sous-cortical sont au centre des préoccupations de plus en plus de chercheurs, avec des applications cliniques potentielles dans les troubles du langage. Cet article présente l’évolution des techniques permettant l’évaluation du traitement neuronal de la parole au niveau du tronc cérébral : d’abord les potentiels évoqués auditifs (PEA) en réponse à des clics, ensuite découverte de la réponse soutenue à la fréquence (RSF), enfin PEA en réponse à des sons de parole (PEASP) ou speech auditory brainstem response. Parce qu’ils permettent l’étude des mécanismes sous-corticaux du traitement des sons complexes, les PEASP apportent une vision objective, non invasive et en temps réel des capacités d’encodage neuronal de chaque individu au niveau du tronc cérébral. Leurs caractéristiques devraient leur permettre d’être utilisés comme marqueurs biologiques d’un déficit de l’encodage sous-cortical de la parole, ainsi que de la rééducation de ce type de déficit chez des personnes présentant des troubles de l’apprentissage et/ou du traitement de l’information auditive.
There is a growing and unprecedented interest in the objective evaluation of the subcortical processes that are involved in speech perception, with potential clinical applications in speech and language impairments. Here, we review the studies illustrating the development of electrophysiological methods for assessing speech encoding in the human brainstem: from the pioneer recordings of click-evoked auditory brainstem responses (ABR), via studies of frequency-following responses (FFR) to the most recent measurements of speech ABR (SABR) or ABR in response to speech sounds. Recent research on SABR has provided new insights in the understanding of subcortical auditory processing mechanisms. The SABR test is an objective and non-invasive tool for assessing individual capacity of speech encoding in the brainstem. SABR characteristics are potentially useful both as a diagnosis tool of speech encoding deficits and as an assessment tool of the efficacy of rehabilitation programs in patients with learning and/or auditory processing disorders.
Selectively eliminating cochlear microphonic contamination from the frequency-following response
1990, Electroencephalography and Clinical Neurophysiology
The frequency-following response (FFR) is the scalp recorded response to low frequency stimuli. As an electrophysiological method for determining auditory threshold, it has application in both clinical and research settings. However, the response is often contaminated with the cochlear microphonic (CM), reflecting the response of outer hair cells, rather than neural generators (i.e., auditory nerve, cochlear nucleus, superior olivary nucleus, inferior colliculus, etc.). The FFR needs to be a purely neural response to establish its clinical and experimental usefulness. The methods applied to date have failed to accomplish this. The present study demonstrates a method of deriving a pure neural response by subtracting a forward masked FFR, which contains only CM, from an unmasked FFR. To confirm that the residual response after forward masking is solely CM, one needs to record two forward masked responses with opposite phase probe stimuli. When the responses are added they will sum to zero only if the residual response with forward masking is pure CM. This study demonstrates that the traditional method for removing CM from FFR, by simple summation of unmasked responses recorded with stimuli of opposite phase, does not accurately reflect the amplitude or frequency of the FFR, while the proposed method provides an accurate assessment of the FFR amplitude free of CM contamination.

View all citing articles on Scopus

View full text

Human frequency-following responses to monaural and binaural stimuliReponses en fonction de la frequence a des stimuli mono et bi-auriculaires chez l'homme

Abstract

Résumé

Brain Res.

Exp. Neurol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Auditory-evoked far fields averaged from the scalp of humans

Brain