Distinct Narrow and Broadband Gamma Responses in Human Visual Cortex

Abstract

High frequency activity (> 30 Hz) in the neocortical local field potential, typically referred to as the 'gamma' range, is thought to have a critical role in visual perception and cognition more broadly. Historically, animal studies recording from visual cortex documented clear narrowband gamma oscillations (NBG; ~20-60 Hz) in response to visual stimuli. However, invasive measurements from human neocortex have highlighted a different broadband or 'high' gamma response (BBG; ~70-150+ Hz). Growing evidence suggests these two forms of gamma response are distinct, but often conceptually or analytically conflated as the same 'gamma' response. Furthermore, recent debate has highlighted that both the occurrence and spectral properties of gamma band activity in visual cortex appears to be dependent on the attributes and class of presented visual stimuli. Using high-density intracranial recordings from human visual cortex, we integrate and extend these findings, dissociating the spectral, temporal and functional properties of NBG and BBG activity. We report results from two experiments, manipulating visual stimulus attributes (contrast-varying gratings) and class (object categories) dissecting the differential properties of NBG and BBG responses. NBG oscillations were only reliably recorded for grating stimuli, while their peak frequency varied with contrast level. Whereas BBG activity was observed in response to all stimulus classes tested, with no systematic change in its spectral features. Temporally, induced NBG was sustained throughout stimulus presentation, in opposition to a more transient response for the BBG. These findings challenge the ubiquity of 'gamma' activity in visual cortex, by clearly dissociating oscillatory and broadband effects. Significance Statement:Neocortical narrowband gamma oscillations (~20-60 Hz) have been implicated in vision and cognition as a mechanism for synchronizing brain regions. Efforts to study this phenomenon have revealed an additional 'high-gamma' range response (~70-150+ Hz), which is broadband and non-oscillatory. These different gamma range activities are often conflated in support of the same functional role. Using invasive recordings from human visual cortex, we show that narrow and broadband gamma can be dissociated by spectral, temporal and functional response properties. While broadband gamma responses were more transient to the presentation of all stimuli, narrowband gamma responses were sustained and only occurred reliably to grating stimuli. These differences have important implications for the study, analysis and interpretation of neocortical gamma range activity. Neocortical gamma oscillations, rhythmic neural population activity in the ~20-60 Hz frequency range, have historically been implicated in visual perception and cognitive processing more generally (1-4). Early theoretical accounts posited that the synchronization of gamma oscillations within visual cortex supported the binding of disparate visual features (3)(4)(5). This view has since been extended to prop...

Potential of on‐scalp MEG: Robust detection of human visual gamma‐band responses

“…Whether and how narrowband and broadband gamma are related still remains an open question (Lachaux et al, ). Broadband gamma is often observed in invasive measurements (e.g., Bartoli et al, ; Cervenka et al, ; Crone et al, ; Crone, Sinai, & Korzeniewska, ; Edwards, Soltani, Deouell, Berger, & Knight, ; Hermes et al, ) but rarely in noninvasive ones.…”

“…One explanation why narrowband, but not broadband, gamma would be well visible in noninvasive recordings is that narrowband gamma may be spatially more coherent than broadband gamma. However, a recent study by Bartoli et al (2019) showed that the sources of narrowband gamma responses to gratings are quite focal. They examined the narrowband gamma responses with high-density ECoG grids in the visual cortex and found that the grating stimulus elicited strong narrowband gamma response across electrodes; however, the phase correlation between the electrode responses decayed fast with an estimated spatial decay constant of 2.3-2.5 mm.…”

Potential of on-scalp MEG: Robust detection of human visual gamma-band responses

“…Broadband gamma is often observed in invasive measurements (e.g. Crone et al, 2001;Edwards et al, 2005;Crone et al, 2006;Cervenka et al, 2013;Hermes et al, 2014;Bartoli et al, 2019) but rarely in noninvasive ones.…”

Local sleep during mind-wandering enhances processes of spatial attention allocation

“…The copyright holder for this preprint (which this version posted June 6, 2020. ; https://doi.org/10.1101/2020.06.05.136374 doi: bioRxiv preprint 21 baseline between and 350 Hz, a fast increasing flank peaking around 200 msec, and a slowly decreasing flank in early visual cortex (Burke et al 2014;Golan et al 2016Golan et al , 2017Gerber et al 2017;Helfrich et al 2018;Bartoli et al 2019). The high similarity of the HFA response across subjects indicates that MEG in contrast to EEG can reliably pick up high frequency activity responses to visual stimuli which even has been shown at the single trial level (Westner et al 2018).…”