Functionally Distinct Gamma Range Activity Revealed by Stimulus Tuning in Human Visual Cortex

Abstract

Highlights d Temporal, spectral, and functional properties dissociate narrow and broadband gamma d Narrowband gamma is tuned to visual gratings and longwavelength hues (red/orange) d Narrowband gamma responses to natural images reflect lowlevel stimulus tuning d Stimulus dependencies limit the functional role of narrowband gamma oscillations SUMMARYNeocortical gamma activity has long been hypothesized as a mechanism for synchronizing brain regions to support visual perception and cognition more broadly. Although early studies focused on narrowband gamma oscillations ($20-60 Hz), recent work has emphasized a more broadband ''high-gamma'' response ($70-150+ Hz). These responses are often conceptually or analytically treated as synonymous markers of gamma activity. Using high-density intracranial recordings from the human visual cortex, we challenge this view by showing distinct spectral, temporal, and functional properties of narrow and broadband gamma. Across four experiments, narrowband gamma was strongly selective for gratings and longwavelength colors, displaying a delayed response onset, sustained temporal profile, and contrastdependent peak frequency. In addition, induced narrowband gamma oscillations lacked phase consistency across stimulus repetitions and displayed highly focal inter-site synchronization. In contrast, broadband gamma was consistently observed for all presented stimuli, displaying a rapid response onset, transient temporal profile, and invariant spectral properties. We exploited stimulus tuning to highlight the functional dissociation of these distinct signals, reconciling prior inconsistencies across species and stimuli regarding the ubiquity of visual gamma oscillations during natural vision. The occurrence of visual narrowband gamma oscillations, unlike broadband high gamma, appears contingent on specific structural and chromatic stimulus attributes intersecting with the receptive field. Together, these findings have important implications for the study, analysis, and functional interpretation of neocortical gammarange activity.

Dynamic Normalization

“…The models exhibited gamma oscillations for a restricted subset of stimulus conditions, depending on the strength of the normalization pool. Consequently, oscillation amplitude was strongest for large, high contrast gratings, and weaker (or non-existent) for other spatial patterns and low contrasts, similar to experimental results (31,(72)(73)(74)(75)(76)(77)(78)(79)(80)(81)(82)(83)(84)(85)(86) Long wavelength stimuli have been found to evoke particularly large amplitude gamma oscillations (85,148). It should be straightforward to extend the current models to account for these results by including red-green and blue-yellow color-opponent channels (149)(150)(151) in the LGN input, and by setting the normalization weights to be large for the red-green channel.…”

“…All of these results, except for one, are commensurate with experimental observations that oscillation amplitudes and frequencies depend systematically on stimulus contrast, size, and spatial pattern (31,(72)(73)(74)(75)(76)(77)(78)(79)(80)(81)(82)(83)(84)(85)(86), and that oscillations are linked to normalization (31,72). Like the simulation results, oscillation amplitudes have been observed to increase with stimulus contrast and size, oscillation frequencies increase with stimulus contrast, and oscillations are smaller for plaids than for gratings (and even smaller for stimuli composed of multiple components, also predicted by the model).…”

“…Narrow-band gamma oscillations have been proposed to play a functional role in stimulus feature binding (127)(128)(129)(130), attention (131)(132)(133)(134), and/or synchronizing neuronal activity to enhance signal transmission and communication between brain areas (130,133,(135)(136)(137)(138)(139)(140)(141)(142). These speculations have been met with considerable skepticism (74,77,79,82,83,(143)(144)(145)(146)(147), in part because oscillation amplitude depends strongly on stimulus conditions (31,(72)(73)(74)(75)(76)(77)(78)(79)(80)(81)(82)(83)(84)(85)(86), incommensurate the perception of those stimulus conditions.…”

“…LFPs exhibit so-called gamma oscillations (~30-80 Hz) that have also been linked to normalization (31,72). Oscillation amplitude and frequency depend systematically on stimulus contrast, size, and spatial pattern (31,(72)(73)(74)(75)(76)(77)(78)(79)(80)(81)(82)(83)(84)(85)(86).…”

Fronto-temporal coupling dynamics during spontaneous activity and auditory processing

“…Short onset-related coherence increase might convey 562 information about the presence of an acoustic stimulus, but not necessarily allow to elucidate the 563 stimulus' spectrotemporal features. In the AC of the bat Pteronotus parnelii, Medvedev and Kanwal 564 (2008) Bartoli et al, 2019). Our stimulus set is not ideal to determine in an unbiased manner whether the 572 nature of FAF-AC gamma synchronization changes given the spectrotemporal characteristics of the 573 stimuli, in particular because LFPs synchronize to a stimulus' temporal structure also in the gamma 574 range (see (Hechavarria et al, 2016b; Garcia-Rosales et al, 2018a).…”