Global and Parallel Cortical Processing Based on Auditory Gamma Oscillatory Responses in Humans

Abstract

Gamma oscillations are physiological phenomena that reflect perception and cognition, and involve parvalbumin-positive γ-aminobutyric acid-ergic interneuron function. The auditory steady-state response (ASSR) is the most robust index for gamma oscillations, and it is impaired in patients with neuropsychiatric disorders such as schizophrenia and autism. Although ASSR reduction is known to vary in terms of frequency and time, the neural mechanisms are poorly understood. We obtained high-density electrocorticography recordings from a wide area of the cortex in 8 patients with refractory epilepsy. In an ASSR paradigm, click sounds were presented at frequencies of 20, 30, 40, 60, 80, 120, and 160 Hz. We performed time-frequency analyses and analyzed intertrial coherence, event-related spectral perturbation, and high-gamma oscillations. We demonstrate that the ASSR is globally distributed among the temporal, parietal, and frontal cortices. The ASSR was composed of time-dependent neural subcircuits differing in frequency tuning. Importantly, the frequency tuning characteristics of the late-latency ASSR varied between the temporal/frontal and parietal cortex, suggestive of differentiation along parallel auditory pathways. This large-scale survey of the cortical ASSR could serve as a foundation for future studies of the ASSR in patients with neuropsychiatric disorders.

Salient 40 Hz sounds probe affective aversion and neural excitability

“…ASSR power averaged across all electrodes showed a sustained response throughout the sound duration (Figure 3a, left panel). Focusing on brain responses to low sounds (30–60 Hz) across all participants (both groups together), we observed that ASSR power in this range was maximal in central and anterior contacts, a topographical pattern that is compatible with the recruitment of auditory and frontal regions as observed in intracranial recordings in humans (5, 18) and murine models (20).…”

“…When studying the neurophysiological origin of the non-linear pattern of aversion across frequencies using intracranial recordings in epileptic patients, we recently suggested that unlike aversion to higher frequencies in the pitch range (>130 Hz), aversion to rough frequencies is best accounted for by the sustained entrainment of activity of brain regions involved in salience and aversion processing (5). In other words, beyond triggering classical onset related potentials (ERPs) in the auditory cortex, the nonlinear effect of subjective aversion in the roughness range is arguably induced by the additional steadystate neural entrainment (ASSR) of widespread non-canonical auditory networks (5,17,18). Considering the disparity of aversion profiles between participants, we then hypothesized that one possible origin of this inter-individual variability might be the relative excitability of these networks and related ASSR responses across participants.…”

“…While some disorders are comorbid with hearing problems (15,16), the prevalence of ASSR impairments in these diseases might point to dysfunctions beyond or outside classical auditory pathways. Indeed, whereas previous EEG studies a priori locate the source of ASSR generators in the auditory cortex, recent findings using alternative reconstruction algorithms or spatially resolved intracranial recordings suggest that rough sounds additionally synchronize non-canonical auditory systems involved in salience and aversion processing (5,17,18). Therefore, impaired ASSR responses -as observed in neuropsychiatric disorders-might actually reflect dysfunctional sensory and emotional processing of exogenous stimulation in these networks.…”

Auditory driven gamma synchrony is associated with cortical thickness in widespread cortical areas

“…We took advantage of auditory entrainment of gamma synchronization over parts of the cortical surface in the temporal and frontal lobes to replicate and expand previous evidence that variations in cortical cell density are involved in the generation of gamma synchrony in widespread cortical regions ( Fig. 3 ) ( Farahani et al., 2021 ; Koshiyama et al., 2020 ; Pellegrino et al., 2019b ; Tada et al., 2021 ).…”

“…Yet, recent evidence suggests that auditory-driven gamma synchronization rather involves the entire cortical mantle. This is supported by whole head EEG and MEG mapping ( Farahani et al., 2021 ; Pellegrino et al., 2019b ), invasive recordings in animal studies ( Cho et al., 2015 , 2020 ) and electrocorticography in epilepsy patients ( Tada et al., 2021 ). As such, exposure to gamma sounds provides a viable way to investigate gamma synchronization of the entire cortical surface.…”