Surprising effects of stimulus repetition on neuronal firing rates and gamma-band synchronization in awake macaque V1

Abstract

Stimulus repetition is abundant, because the environment is redundant and/or because it is redundantly sampled. This offers an opportunity to optimize the processing of repeated stimuli. Indeed, stimulus repetition leads to classically described neuronal response decreases, and to more recently described neuronal gamma synchronization increases (sometimes preceded by decreases for a few trials). Here, we used a full-screen colored background (FSCB) and a flashed black bar, while recording multi-unit activity (MUA) and local field potentials (LFP) from area V1 of an awake macaque monkey. We found that the FSCB repetition induced neuronal response increases (sometimes preceded by decreases for a few trials) and gamma synchronization decreases (preceded by increases for a few trials). These effects are largely opposite to the dominant previous findings. Intriguingly, these surprising effects reversed when we isolated the responses to the flashed black bar. We discuss these findings, considering differences to previous studies with regards to the subject of the study, the stimuli and the task. We notice that in studies reporting classical results for gamma, sometimes in combination with firing rates, the stimuli were typically (partly) predictive of the reward. Here, we found non-classical results for the FSCB that was not reward predictive, and classical results for the black bar that was reward predictive. Whether this has revealed a general effect of reward predictive versus non-predictive stimuli will require further investigation with stimuli and task designs tailored specifically for this question. SignificanceNatural visual experience often entails repetitions of the same stimulus. This allows optimization of the brains processing of those stimuli. Indeed, repeated stimuli typically induce decreasing firing rates and increasing gamma-band synchronization in many visual areas. However, in this study in awake macaque primary visual cortex, we report surprising opposite effects: under some conditions, stimulus repetition can result in neuronal firing rate increases and gamma-band synchronization decreases. We argue that these effects might relate to the fact that the repeated stimulus was not predictive of a reward. In fact, when we isolated the responses to a second stimulus that was added later in each trial and that was predictive of reward, the effects reverted again to the typical pattern.