Distinct Narrow and Broadband Gamma Responses in Human Visual Cortex

Abstract

AbstractHigh 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 StatementNeocortical 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.