Spontaneous network activity <35 Hz accounts for variability in stimulus-induced gamma responses

Abstract

Gamma activity is thought to serve several cognitive processes, including attention and memory. Even for the simplest stimulus, the occurrence of gamma activity is highly variable, both within and between individuals. The sources of this variability are largely unknown. They are, however, critical to deepen our understanding of the relation between gamma activity and behavior.In this paper, we address one possible cause of this variability: the cross-frequency influence of spontaneous, whole-brain network activity on visual stimulus processing. By applying Hidden Markov modelling to MEG data, we reveal that the trial-averaged gamma response to a moving grating depends on the individual network profile, inferred from slower brain activity (<35 Hz) in the absence of stimulation (resting-state and task baseline). In addition, we demonstrate that dynamic modulations of this network activity in task baseline bias the gamma response on the level of trials.In summary, our results reveal a cross-frequency and cross-session association between gamma responses induced by visual stimulation and spontaneous network activity.characterized by a unique spatio-spectral profile within the frequency ranges slower than gamma (1-35 Hz), including the topography of delta power shown here for states 2 (left) and 4 (right). Lower right: The inward-moving grating induced strong gamma activity in occipital areas. We investigated whether the strength of this stimulus-induced gamma response is related to spontaneously occurring whole-brain states. Methods Experimental DesignParticipants 15 healthy participants were recruited for this study (21-45 years; 5 female). The study was approved by the Montreal Neurological Institute's ethics committee (NEU 011-036) and was in accordance with the Declaration of Helsinki. All participants gave written informed consent and were compensated for their participation. ParadigmSubjects were presented with a modified version of the visual stimulation paradigm by Hoogenboom et al. (Hoogenboom et al., 2006): An inward-moving, circular sine wave grating with a diameter of 5° accelerated from 1.6 deg/s to 2.2 deg/s at an unpredictable moment between 3-5 seconds after stimulus onset. Subjects indicated that they had detected the velocity change by pressing a button with the index finger of the dominant hand. The button press ended the trial and the stimulus was turned off. During the inter-trial interval (baseline period), subjects were presented with a central fixation cross. Inter-trial intervals varied between 2 and 4s. A few trials with longer interval (17 -19 s) were randomly interspersed in the trial sequence for all subjects but P1 (6 -16 per subject; mean: 13). This was done to facilitate an analysis of the influence of baseline duration, but is not relevant for the analyses reported here. Experimental ProcedureEach session started with a 5 min resting-state recording with eyes open, which was immediately followed by task practice and task recording. Before the start of the reaction time task, participa...