Independent predictors of neuronal adaptation in human primary visual cortex measured with high-gamma activity

Abstract

Neuronal adaptation is defined as a reduced neural response to a repeated stimulus and can be demonstrated by reduced augmentation of event-related gamma activity. Several studies reported that variance in the degree of gamma augmentation could be explained by pre-stimulus low-frequency oscillations. Here, we measured the spatio-temporal characteristics of visually-driven amplitude modulations in human primary visual cortex using intracranial electrocorticography. We determined if inter-stimulus intervals or pre-stimulus oscillations independently predicted local neuronal adaptation measured with amplitude changes of high-gamma activity at 80-150 Hz. Participants were given repetitive photic stimuli with a flash duration of 20 μs in each block; the inter-stimulus interval was set constant within each block but different (0.2, 0.5, 1.0 or 2.0s) across blocks. Stimuli elicited augmentation of high-gamma activity in the occipital cortex at about 30 to 90 ms, and high-gamma augmentation was most prominent in the medial occipital region. High-gamma augmentation was subsequently followed by lingering beta augmentation at 20-30 Hz and high-gamma attenuation. Neuronal adaptation was demonstrated as a gradual reduction of high-gamma augmentation over trials. Multivariate analysis demonstrated that a larger number of prior stimuli, shorter inter-stimulus interval, and pre-stimulus high-gamma attenuation independently predicted a reduced high-gamma augmentation in a given trial, while pre-stimulus beta amplitude or delta phase had no significant predictive value. Association between pre-stimulus high-gamma attenuation and a reduced neural response suggests that high-gamma attenuation represents a refractory period. The local effects of pre-stimulus beta augmentation and delta phase on neuronal adaptation may be modest in primary visual cortex.