Far-field recorded frequency-following responses: Evidence for the locus of brainstem sources

doi:10.1016/0013-4694(75)90047-4

Electroencephalography and Clinical Neurophysiology

Volume 39, Issue 5, November 1975, Pages 465-472

https://doi.org/10.1016/0013-4694(75)90047-4 Get rights and content

Abstract

Two experiments were performed to determine the brainstem origins of the scalp recorded auditory frequency-following response (FFR). The first was a study of FFR onset latency in which responses observed by direct recording from depth electrodes in brainstem auditory nuclei were compared with those obtained from the scalp. The mean onset latency of scalp recorded FFR (5.8 msec) closely approximated the 5.4 msec mean latency of response recorded from within the inferior colliculus (IC). In a second experiment, cooling of the IC greatly reduced or eliminated FFR both within this nucleus and at the scalp. FFR at the medial superior olive was unaffected during cooling. It was concluded that at moderate intensities of stimulation the primary source of scalp recorded FFR is the IC.

Résumé

Deux types d'expériences ont été réalisés pour déterminer les origines, au niveau du tronc cérébral, de la réponse d'entrainement auditif enregistrée sur le scalp (FFR). La première est l'étude de la latence du début du FFR dans laquelle les réponses observées par enregistrement direct sur des électrodes profondes situées dans les noyaux auditifs du tronc cérébral étaient comparées à celles obtenues sur le scalp. La latence moyenne de début des FFR enregistrées sur le scalp (5.8 msec) est très proche de la latence moyenne de 5.4 msec de la réponse enregistrée au niveau du colliculus inférieur (IC). Dans une seconde expérience, la réfrigération du IC réduit grandement ou élimine les FFR à la fois à l'intérieur de ce noyau et au niveau du scalp. La FFR au niveau de l'olive médiane supérieure n'est pas affectée par cette réfrigération. L'auteur conclue qu'à des intensités modérées de stimulation la source primaire du FFR enregistré sur le scalp est l'IC.

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Pitch is a perceptual rather than physical phenomenon, important for spoken language use, musical communication, and other aspects of everyday life. Auditory stimuli can be designed to probe the relationship between perception and physiological responses to pitch-evoking stimuli. One technique for measuring physiological responses to pitch-evoking stimuli is the frequency following response (FFR). The FFR is an electroencephalographic (EEG) response to periodic auditory stimuli. The FFR contains nonlinearities not present in the stimuli, including correlates of the amplitude envelope of the stimulus; however, these nonlinearities remain undercharacterized. The FFR is a composite response reflecting multiple neural and peripheral generators, and their contributions to the scalp-recorded FFR vary in ill-understood ways depending on the electrode montage, stimulus, and imaging technique. The FFR is typically assumed to be generated in the auditory brainstem; there is also evidence both for and against a cortical contribution to the FFR. Here a methodology is used to examine the FFR correlates of pitch and the generators of the FFR to stimuli with different pitches. Stimuli were designed to tease apart biological correlates of pitch and amplitude envelope. FFRs were recorded with 256-electrode EEG nets, in contrast to a typical FFR setup which only contains a single active electrode. Structural MRI scans were obtained for each participant to co-register with the electrode locations and constrain a source localization algorithm. The results of this localization shed light on the generating mechanisms of the FFR, including providing evidence for both cortical and subcortical auditory sources.
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The brain transforms continuous acoustic events into discrete category representations to downsample the speech signal for our perceptual-cognitive systems. Such phonetic categories are highly malleable, and their percepts can change depending on surrounding stimulus context. Previous work suggests these acoustic-phonetic mapping and perceptual warping of speech emerge in the brain no earlier than auditory cortex. Here, we examined whether these auditory-category phenomena inherent to speech perception occur even earlier in the human brain, at the level of auditory brainstem. We recorded speech-evoked frequency following responses (FFRs) during a task designed to induce more/less warping of listeners’ perceptual categories depending on stimulus presentation order of a speech continuum (random, forward, backward directions). We used a novel clustered stimulus paradigm to rapidly record the high trial counts needed for FFRs concurrent with active behavioral tasks. We found serial stimulus order caused perceptual shifts (hysteresis) near listeners’ category boundary confirming identical speech tokens are perceived differentially depending on stimulus context. Critically, we further show neural FFRs during active (but not passive) listening are enhanced for prototypical vs. category-ambiguous tokens and are biased in the direction of listeners’ phonetic label even for acoustically-identical speech stimuli. These findings were not observed in the stimulus acoustics nor model FFR responses generated via a computational model of cochlear and auditory nerve transduction, confirming a central origin to the effects. Our data reveal FFRs carry category-level information and suggest top-down processing actively shapes the neural encoding and categorization of speech at subcortical levels. These findings suggest the acoustic-phonetic mapping and perceptual warping in speech perception occur surprisingly early along the auditory neuroaxis, which might aid understanding by reducing ambiguity inherent to the speech signal.
Brainstem speech encoding is dynamically shaped online by fluctuations in cortical α state
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Experimental evidence in animals demonstrates cortical neurons innervate subcortex bilaterally to tune brainstem auditory coding. Yet, the role of the descending (corticofugal) auditory system in modulating earlier sound processing in humans during speech perception remains unclear. Here, we measured EEG activity as listeners performed speech identification tasks in different noise backgrounds designed to tax perceptual and attentional processing. We hypothesized brainstem speech coding might be tied to attention and arousal states (indexed by cortical $α$ power) that actively modulate the interplay of brainstem-cortical signal processing. When speech-evoked brainstem frequency-following responses (FFRs) were categorized according to cortical $α$ states, we found low $α$ FFRs in noise were weaker, correlated positively with behavioral response times, and were more ”decodable” via neural classifiers. Our data provide new evidence for online corticofugal interplay in humans and establish that brainstem sensory representations are continuously yoked to (i.e., modulated by) the ebb and flow of cortical states to dynamically update perceptual processing.
Age-related reduction in frequency-following responses as a potential marker of cochlear neural degeneration
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Healthy aging may be associated with neural degeneration in the cochlea even before clinical hearing loss emerges. Reduction in frequency-following responses (FFRs) to tonal carriers in older clinically normal-hearing listeners has previously been reported, and has been argued to reflect an age-dependent decline in temporal processing in the central auditory system. Alternatively, age-dependent loss of auditory nerve fibers (ANFs) may have little effect on audiometric sensitivity and yet compromise the precision of neural phase-locking relying on joint activity across populations of fibers. This peripheral loss may, in turn, contribute to reduced neural synchrony in the brainstem as reflected in the FFR. Here, we combined human electrophysiology and auditory nerve (AN) modeling to investigate whether age-related changes in the FFR would be consistent with peripheral neural degeneration. FFRs elicited by pure tones and frequency sweeps at carrier frequencies between 200 and 1200 Hz were obtained in older (ages 48–76) and younger (ages 20–30) listeners, both groups having clinically normal audiometric thresholds up to 6 kHz. The same stimuli were presented to a computational model of the AN in which age-related loss of hair cells or ANFs was modelled using human histopathological data. In the older human listeners, the measured FFRs to both sweeps and pure tones were found to be reduced across the carrier frequencies examined. These FFR reductions were consistent with model simulations of age-related ANF loss. In model simulations, the phase-locked response produced by the population of remaining fibers decreased proportionally with increasing loss of the ANFs. Basal-turn loss of inner hair cells also reduced synchronous activity at lower frequencies, albeit to a lesser degree. Model simulations of age-related threshold elevation further indicated that outer hair cell dysfunction had no negative effect on phase-locked AN responses. These results are consistent with a peripheral source of the FFR reductions observed in older normal-hearing listeners, and indicate that FFRs at lower carrier frequencies may potentially be a sensitive marker of peripheral neural degeneration.
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The frequency-following response (FFR) to periodic complex sounds has gained recent interest in auditory cognitive neuroscience as it captures with great fidelity the tracking accuracy of the periodic sound features in the ascending auditory system. Seminal studies suggested the FFR as a correlate of subcortical sound encoding, yet recent studies aiming to locate its sources challenged this assumption, demonstrating that FFR receives some contribution from the auditory cortex. Based on frequency-specific phase-locking capabilities along the auditory hierarchy, we hypothesized that FFRs to higher frequencies would receive less cortical contribution than those to lower frequencies, hence supporting a major subcortical involvement for these high frequency sounds. Here, we used a magnetoencephalographic (MEG) approach to trace the neural sources of the FFR elicited in healthy adults (N = 19) to low (89 Hz) and high (333 Hz) frequency sounds. FFRs elicited to the high and low frequency sounds were clearly observable on MEG and comparable to those obtained in simultaneous electroencephalographic recordings. Distributed source modeling analyses revealed midbrain, thalamic, and cortical contributions to FFR, arranged in frequency-specific configurations. Our results showed that the main contribution to the high-frequency sound FFR originated in the inferior colliculus and the medial geniculate body of the thalamus, with no significant cortical contribution. In contrast, the low-frequency sound FFR had a major contribution located in the auditory cortices, and also received contributions originating in the midbrain and thalamic structures. These findings support the multiple generator hypothesis of the FFR and are relevant for our understanding of the neural encoding of sounds along the auditory hierarchy, suggesting a hierarchical organization of periodicity encoding.

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^☆: This research was supported by NIMH Grant MH-03831.

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Far-field recorded frequency-following responses: Evidence for the locus of brainstem sourcesReponses d'entrainement enregistrees a distance: Preuves en faveur de leur origine au niveau du tronc cerebral☆

Abstract

Résumé

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.