Stimulus-specific plasticity in human visual gamma-band activity and functional connectivity.

Benjamin J Stauch,Alina Peter,Heike Schuler,Pascal Fries

doi:10.7554/elife.68240

Abstract

Under natural conditions, the visual system often sees a given input repeatedly. This provides an opportunity to optimize processing of the repeated stimuli. Stimulus repetition has been shown to strongly modulate neuronal-gamma band synchronization, yet crucial questions remained open. Here we used magnetoencephalography in 30 human subjects and find that gamma decreases across ≈10 repetitions and then increases across further repetitions, revealing plastic changes of the activated neuronal circuits. Crucially, increases induced by one stimulus did not affect responses to other stimuli, demonstrating stimulus specificity. Changes partially persisted when the inducing stimulus was repeated after 25 minutes of intervening stimuli. They were strongest in early visual cortex and increased interareal feedforward influences. Our results suggest that early visual cortex gamma synchronization enables adaptive neuronal processing of recurring stimuli. These and previously reported changes might be due to an interaction of oscillatory dynamics with established synaptic plasticity mechanisms.

Highlights

While moving through natural environments, organisms rarely encounter random and temporally independent visual inputs
Stimulus repetition has been shown to lead to a reduction of firing rates in stimulus-driven neurons (Desimone, 1996; Li et al, 1993) and a decreased hemodynamic response (Grill-Spector et al, 2006; Stern et al, 1996) in visual areas, a phenomenon generally called repetition suppression
The gamma-power enhancement across stimulus repetitions partially persisted over more than 25 minutes of intervening presentation of other orientations: Induced gamma power during block A2 was on average a further 7.80 pp above the level predicted by all other factors

Summary

Introduction

While moving through natural environments, organisms rarely encounter random and temporally independent visual inputs. Stimulus repetition has been shown to lead to a reduction of firing rates in stimulus-driven neurons (Desimone, 1996; Li et al, 1993) and a decreased hemodynamic response (Grill-Spector et al, 2006; Stern et al., 1996) in visual areas, a phenomenon generally called repetition suppression This decrease of neuronal activity does not lead to decreases in detection performance. Behavior might rely primarily on the neurons most responsive to the repeated input, which might be exempted from repetition suppression (Desimone, 1996; Homann et al, 2017) or might even undergo repetition enhancement (Lim et al., 2015) Consistent with the latter, a further possibility is that the remaining, non-suppressed neurons fire more synchronously, effectively compensating for decreased firing rates via increased temporal overlap between action potentials (Gotts et al, 2012). We found that the repetition-related gamma enhancement effect is clearly present in humans, is stimulus-specific, and persists over time and deadaptation

Results

Discussion

Participants