Precise Spatiotemporal Patterns among Visual Cortical Areas and Their Relation to Visual Stimulus Processing

Abstract

Visual processing shows a highly distributed organization in which the presentation of a visual stimulus simultaneously activates neurons in multiple columns across several cortical areas. It has been suggested that precise spatiotemporal activity patterns within and across cortical areas play a key role in higher cognitive, motor, and visual functions. In the visual system, these patterns have been proposed to take part in binding stimulus features into a coherent object, i.e., to be involved in perceptual grouping. Using voltage-sensitive dye imaging (VSDI) in behaving monkeys (Macaca fascicularis, males), we simultaneously measured neural population activity in the primary visual cortex (V1) and extrastriate cortex (V2, V4) at high spatial and temporal resolution. We detected time point population events (PEs) in the VSDI signal of each pixel and found that they reflect transient increased neural activation within local populations by establishing their relation to spiking and local field potential activity. Then, we searched for repeating space and time relations between the detected PEs. We demonstrate the following: (1) spatiotemporal patterns occurring within (horizontal) and across (vertical) early visual areas repeat significantly above chance level; (2) information carried in only a few patterns can be used to reliably discriminate between stimulus categories on a single-trial level; (3) the spatiotemporal patterns yielding high classification performance are characterized by late temporal occurrence and top-down propagation, which are consistent with cortical mechanisms involving perceptual grouping. The pattern characteristics and the robust relation between the patterns and the stimulus categories suggest that spatiotemporal activity patterns play an important role in cortical mechanisms of higher visual processing.