Distinct oscillatory patterns differentiate between segregation and integration processes in perceptual grouping

Abstract

Recently, there has been a resurgence in experimental and conceptual efforts to understand how brain rhythms can serve to organize visual information. Oscillations can provide temporal structure for neuronal processing and form a basis for integrating information across brain areas. Here, we use a bistable paradigm and a data-driven approach to test the hypothesis that oscillatory modulations associate with the integration or segregation of visual elements. Spectral signatures of perception of bound and unbound configurations of visual moving stimuli were studied using magnetoencephalography (MEG) in ambiguous and unambiguous conditions. Using a 2 × 2 design, we were able to isolate correlates from visual integration, either perceptual or stimulus-driven, from attentional and ambiguity-related activity. Two frequency bands were found to be modulated by visual integration: an alpha/beta frequency and a higher frequency gamma-band. Alpha/beta power was increased in several early visual cortical and dorsal visual areas during visual integration, while gamma-band power was surprisingly increased in the extrastriate visual cortex during segregation. This points to an integrative role for alpha/beta activity, likely from top-down signals maintaining a single visual representation. On the other hand, when more representations have to be processed in parallel gamma-band activity is increased, which is at odds with the notion that gamma oscillations are related to perceptual coherence. These modulations were confirmed in intracranial EEG recordings and partially originate from distinct brain areas. Our MEG and stereo-EEG data confirms predictions of binding mechanisms depending on low-frequency activity for long-range integration and for organizing visual processing while refuting a straightforward correlation between gamma-activity and perceptual binding. PRACTITIONER POINTS: Distinct neurophysiological signals underlie competing bistable percepts. Increased alpha/beta activity correlate with visual integration while gamma correlates with segmentation. Ambiguous percepts drive alpha/beta activity in the posterior cingulate cortex.