Case studies in neuroscience: Cortical contributions to the frequency-following response depend on subcortical synchrony

Journal of Neurophysiology ◽

10.1152/jn.00104.2020 ◽

2020 ◽

Author(s):

Travis White-Schwoch ◽

Jennifer Krizman ◽

Trent Nicol ◽

Nina Kraus

Keyword(s):

Auditory Cortex ◽

Control Subject ◽

Case Studies ◽

Fundamental Frequency ◽

Auditory Neuropathy ◽

Neural Synchrony ◽

Frequency Following Response ◽

Onset Responses

Frequency-following responses to musical notes spanning the octave 65-130 Hz were elicited in a person with auditory neuropathy, a disorder of subcortical neural synchrony, and a control subject. No phaselocked responses were observed in the person with auditory neuropathy. The control subject had robust responses synchronized to the fundamental frequency and its harmonics. Cortical onset responses to each note in the series were present in both subjects. These results support the hypothesis that subcortical neural synchrony is necessary to generate the frequency-following response-including for stimulus frequencies at which a cortical contribution has been noted. Although auditory cortex ensembles may synchronize to fundamental frequency cues in speech and music, subcortical neural synchrony appears to be a necessary antecedent.

Download Full-text

Cortical correlates of the auditory frequency-following and onset responses: EEG and fMRI evidence

10.1101/076448 ◽

2016 ◽

Author(s):

Emily B.J. Coffey ◽

Gabriella Musacchia ◽

Robert J. Zatorre

Keyword(s):

Individual Differences ◽

Auditory Cortex ◽

Fundamental Frequency ◽

Initial Response ◽

Cortical Activity ◽

Acoustic Energy ◽

Frequency Following Response ◽

Auditory Cognition ◽

Brainstem Nuclei ◽

The Right

AbstractThe frequency following response (FFR) is a measure of the brain’s periodic sound encoding. It is of increasing importance for studying the human auditory nervous system due to numerous associations with auditory cognition and dysfunction. Although the FFR is widely interpreted as originating from brainstem nuclei, a recent study using magnetoencephalography (MEG) suggested that there is also a right-lateralized contribution from the auditory cortex at the fundamental frequency (Coffey et al., 2016c). Our objectives in the present work were to validate and better localize this result using a completely different neuroimaging modality, and document the relationships between the FFR and the onset response, and cortical activity. Using a combination of electroencephalography, fMRI, and diffusion-weighted imaging, we show that activity in the right auditory cortex is related to individual differences in FFR-f0 strength, a finding that was replicated with two independent stimulus sets, with and without acoustic energy at the fundamental frequency. We demonstrate a dissociation between this FFR-f0-sensitive response in the right and an area in left auditory cortex that is sensitive to individual differences in the timing of initial response to sound onset. Relationships to timing and their lateralization are supported by parallels in the microstructure of the underlying white matter, implicating a mechanism involving neural conduction efficiency. These data confirm that the FFR has a cortical contribution, and suggest ways in which auditory neuroscience may be advanced by connecting early sound representation to measures of higher-level sound processing and cognitive function.Significance StatementThe frequency following response (FFR) is an electroencephalograph signal that is used to explore how the auditory system encodes temporal regularities in sound, and which is related to differences in auditory function between individuals. It is known that brainstem nuclei contribute to the FFR, but recent findings of an additional cortical source are more controversial. Here, we use functional MRI to validate and extend the prediction from magnetoencephalography data of a right auditory cortex contribution to the FFR. We also demonstrate a dissociation between FFR-related cortical activity from that related to the latency of the response to sound onset, which is found in left auditory cortex. The findings provide a clearer picture of cortical processes for analysis of sound features.

Download Full-text

Multiple Cases of Auditory Neuropathy Illuminate the Importance of Subcortical Neural Synchrony for Speech-in-noise Recognition and the Frequency-following Response

Ear and Hearing ◽

10.1097/aud.0000000000001122 ◽

2021 ◽

Vol Publish Ahead of Print ◽

Author(s):

Travis White-Schwoch ◽

Samira Anderson ◽

Jennifer Krizman ◽

Silvia Bonacina ◽

Trent Nicol ◽

...

Keyword(s):

Auditory Neuropathy ◽

Neural Synchrony ◽

Frequency Following Response ◽

Speech In Noise

Download Full-text

Case studies in neuroscience: subcortical origins of the frequency-following response

Journal of Neurophysiology ◽

10.1152/jn.00112.2019 ◽

2019 ◽

Vol 122 (2) ◽

pp. 844-848 ◽

Cited By ~ 7

Author(s):

Travis White-Schwoch ◽

Samira Anderson ◽

Jennifer Krizman ◽

Trent Nicol ◽

Nina Kraus

Keyword(s):

Auditory Cortex ◽

Neural Activity ◽

Auditory Pathway ◽

Auditory Neuropathy ◽

Frequency Following Response ◽

Double Dissociation ◽

Cortical Responses ◽

Necessary And Sufficient ◽

Dual Case

The auditory frequency-following response (FFR) reflects synchronized and phase-locked activity along the auditory pathway in response to sound. Although FFRs were historically thought to reflect subcortical activity, recent evidence suggests an auditory cortex contribution as well. Here we present electrophysiological evidence for the FFR’s origins from two cases: a patient with bilateral auditory cortex lesions and a patient with auditory neuropathy, a condition of subcortical origin. The patient with auditory cortex lesions had robust and replicable FFRs, but no cortical responses. In contrast, the patient with auditory neuropathy had no FFR despite robust and replicable cortical responses. This double dissociation shows that subcortical synchrony is necessary and sufficient to generate an FFR. NEW & NOTEWORTHY The frequency-following response (FFR) reflects synchronized and phase-locked neural activity in response to sound. The authors present a dual case study, comparing FFRs and cortical potentials between a patient with auditory neuropathy (a condition of subcortical origin) and a patient with bilateral auditory cortex lesions. They show that subcortical synchrony is necessary and sufficient to generate an FFR.

Download Full-text

Neural interaction in cat primary auditory cortex II. Effects of sound stimulation

Journal of Neurophysiology ◽

10.1152/jn.1994.71.1.246 ◽

1994 ◽

Vol 71 (1) ◽

pp. 246-270 ◽

Cited By ~ 64

Author(s):

J. J. Eggermont

Keyword(s):

Auditory Cortex ◽

Cortical Neurons ◽

Relative Size ◽

Primary Auditory Cortex ◽

Mean Value ◽

Neural Synchrony ◽

Sound Stimulation ◽

Common Input ◽

Neural Correlation ◽

The Mean

1. The effect of auditory stimulation with click trains, noise bursts, amplitude-modulated noise bursts, and amplitude-modulated tone bursts on the correlation of firing of 1,290 neuron pairs recorded on one or two electrodes in primary auditory cortex of the cat was investigated. A distinction was made between neural synchrony (the correlation under stimulus conditions) and neural correlation (the correlation under spontaneous or under stimulus conditions after correction for stimulus-related correlations). For neural correlation 63% of the single-electrode pairs showed a unilateral excitation component, often combined with a common-input peak, and only 11% of the dual electrode pairs showed this unilateral excitation. 2. Under poststimulus conditions the incidence of correlograms with clear peaks was high for single-electrode pairs (80–90% range) and somewhat lower for dual-electrode pairs (50–60% range). The strength of the neural correlation for poststimulus conditions, from 0.5 to 2 s after a 1-s stimulus, was comparable with that obtained for 15-min continuous silence, suggesting that aftereffects of stimulation had largely disappeared after 0.5 s. A stationary analysis of the correlation coefficient corroborated this. 3. Two stimulus-correction procedures, one based on the shift predictor and the other based on the joint peristimulus-time histogram (JPSTH) were compared. The mean value of the neural correlation under stimulus conditions obtained after applying the poststimulus time (PST) predictor was on average 20% larger than the mean value obtained after application of the shift predictor; however, this was not significantly different at the 0.05 level. There were no differences in the shape of the correlograms. This suggests that the less time-consuming shift predictor-based stimulus-correction procedure can be used for cortical neurons. 4. Under stimulus conditions neural correlation coefficients could be < or = 50% smaller than for spontaneous conditions. The strength of the stimulus-corrected neural correlation was inversely related to the relative size of the stimulus predictor (compared with the neural synchrony) and thus to the effectiveness of stimulation. This suggests that the assumption of additivity of stimulus and connectivity effects on neural synchrony is generally violated both for shift predictor and PST predictor procedures. 5. The neural correlogram peaks were narrower for single-electrode pairs than for dual-electrode pairs both under stimulus and spontaneous conditions. Under stimulus conditions the peaks were generally narrower than under spontaneous firing conditions.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

Cortical Auditory Evoked Potentials in the Assessment of Auditory Neuropathy: Two Case Studies

Journal of the American Academy of Audiology ◽

10.3766/jaaa.18.5.3 ◽

2007 ◽

Vol 18 (05) ◽

pp. 380-390 ◽

Cited By ~ 26

Author(s):

Wendy Pearce ◽

Maryanne Golding ◽

Harvey Dillon

Keyword(s):

Evoked Potentials ◽

Case Studies ◽

Auditory Evoked Potentials ◽

Auditory Neuropathy ◽

Auditory Brainstem Responses ◽

Cochlear Function ◽

Screening Programs ◽

Young Infants ◽

Brainstem Function ◽

Cortical Auditory Evoked Potentials

Infants with auditory neuropathy and possible hearing impairment are being identified at very young ages through the implementation of hearing screening programs. The diagnosis is commonly based on evidence of normal cochlear function but abnormal brainstem function. This lack of normal brainstem function is highly problematic when prescribing amplification in young infants because prescriptive formulae require the input of hearing thresholds that are normally estimated from auditory brainstem responses to tonal stimuli. Without this information, there is great uncertainty surrounding the final fitting. Cortical auditory evoked potentials may, however, still be evident and reliably recorded to speech stimuli presented at conversational levels. The case studies of two infants are presented that demonstrate how these higher order electrophysiological responses may be utilized in the audiological management of some infants with auditory neuropathy. Los niños con neuropatía auditiva y posibles posibles trastornos auditivos están siendo identificados a edades tempranas con la implementación de programas de tamizaje auditivo. El diagnóstico se basa en la evidencia de una función coclear normal pero de una función anormal del tallo cerebral. Esta falta de función normal de tallo cerebral es muy problemática cuando se trata de prescribir amplificación en niños pequeños, porque las fórmulas de prescripción requieren el insumo de los umbrales auditivos que se estiman normalmente a partir de las respuestas del tallo cerebral ante estímulos tonales. Sin esta información, existe una gran incertidumbre en cuanto a la adaptación final. Los potenciales evocados auditivos corticales pueden, sin embargo, registrarse con confiabilidad a partir de estímulos de lenguaje presentados a niveles de intensidad para la conversación. Se presenta el estudio de dos casos de niños, que demuestran como estas respuestas electrofisiológicas de orden mayor pueden utilizarse en el manejo audiológico de algunos niños con neuropatía auditiva.

Download Full-text

Speech frequency-following response in human auditory cortex is more than a simple tracking

NeuroImage ◽

10.1016/j.neuroimage.2020.117545 ◽

2021 ◽

Vol 226 ◽

pp. 117545

Author(s):

Ning Guo ◽

Xiaopeng Si ◽

Yang Zhang ◽

Yue Ding ◽

Wenjing Zhou ◽

...

Keyword(s):

Auditory Cortex ◽

Frequency Following Response ◽

Human Auditory Cortex

Download Full-text

Coding of Repetitive Transients by Auditory Cortex on Heschl's Gyrus

Journal of Neurophysiology ◽

10.1152/jn.91346.2008 ◽

2009 ◽

Vol 102 (4) ◽

pp. 2358-2374 ◽

Cited By ~ 109

Author(s):

John F. Brugge ◽

Kirill V. Nourski ◽

Hiroyuki Oya ◽

Richard A. Reale ◽

Hiroto Kawasaki ◽

...

Keyword(s):

Auditory Cortex ◽

Intractable Epilepsy ◽

Primate Species ◽

Frequency Following Response ◽

Depth Electrodes ◽

Heschl’S Gyrus ◽

Long Latency ◽

Surgical Evaluation ◽

Latency Response ◽

Heschl's Gyrus

The capacity of auditory cortex on Heschl's gyrus (HG) to encode repetitive transients was studied in human patients undergoing surgical evaluation for medically intractable epilepsy. Multicontact depth electrodes were chronically implanted in gray matter of HG. Bilaterally presented stimuli were click trains varying in rate from 4 to 200 Hz. Averaged evoked potentials (AEPs) and event-related band power (ERBP), computed from responses at each of 14 recording sites, identified two auditory fields. A core field, which occupies posteromedial HG, was characterized by a robust polyphasic AEP on which could be superimposed a frequency following response (FFR). The FFR was prominent at click rates below ∼50 Hz, decreased rapidly as click rate was increased, but could reliably be detected at click rates as high as 200 Hz. These data are strikingly similar to those obtained by others in the monkey under essentially the same stimulus conditions, indicating that mechanisms underlying temporal processing in the auditory core may be highly conserved across primate species. ERBP, which reflects increases or decreases of both phase-locked and non–phase-locked power within given frequency bands, showed stimulus-related increases in gamma band frequencies as high as 250 Hz. The AEPs recorded in a belt field anterolateral to the core were typically of low amplitude, showing little or no evidence of short-latency waves or an FFR, even at the lowest click rates used. The non–phase-locked component of the response extracted from the ERBP showed a robust, long-latency response occurring here in response to the highest click rates in the series.

Download Full-text

Parallels Between Timing of Onset Responses of Single Neurons in Cat and of Evoked Magnetic Fields in Human Auditory Cortex

Journal of Neurophysiology ◽

10.1152/jn.2000.84.5.2426 ◽

2000 ◽

Vol 84 (5) ◽

pp. 2426-2439 ◽

Cited By ~ 60

Author(s):

Silke Biermann ◽

Peter Heil

Keyword(s):

Magnetic Fields ◽

Auditory Cortex ◽

Rise Time ◽

Cortical Neurons ◽

Single Neuron ◽

Dynamic Properties ◽

Threshold Model ◽

Single Neurons ◽

Response Timing ◽

Onset Responses

Sound onsets constitute particularly salient transients and evoke strong responses from neurons of the auditory system, but in the past, such onset responses have often been analyzed with respect to steady-state features of sounds, like the sound pressure level. Recent electrophysiological studies of single neurons from the auditory cortex of anesthetized cats have revealed that the timing and strength of onset responses are shaped by dynamic stimulus properties at their very onsets. Here we demonstrate with magnetoencephalography that stimulus-response relationships very similar to those of the single neurons are observed in two onset components, N100m and P50m, of auditory evoked magnetic fields (AEFs) from the auditory cortex of awake humans. In response to tones shaped with cosine-squared rise functions, N100m and P50m peak latencies vary systematically with tone level and rise time but form a rather invariant function of the acceleration of the envelope at tone onset. Hence N100m and P50m peak latencies, as well as peak amplitudes, are determined by dynamic properties of the stimuli within the first few milliseconds, though not necessarily by acceleration. The changes of N100m and P50m peak latencies with rise time and level are incompatible with a fixed-amplitude threshold model. The direct comparison of the neuromagnetic and single-neuron data shows that, on average, the variance of the neuromagnetic data is larger by one to two orders of magnitude but that favorable measurements can yield variances as low as those derived from neurons with mediocre precision of response timing. The striking parallels between the response timing of single cortical neurons and of AEFs provides a stronger link between single neuron and population activity.

Download Full-text