Rapid recurrent processing gates awareness in primary visual cortex

Abstract

Visual awareness has been proposed to depend on recurrent processing in early visual cortex areas including the primary visual cortex (V1). Here, we address this hypothesis with high spatiotemporal resolution magnetoencephalographic recordings in subjects performing a substitution masking paradigm. Neural activity reflecting awareness is assessed by directly comparing the neuromagnetic response elicited by effectively and ineffectively masked targets after the proportion of trials leading to masking was individually adjusted to match the proportion of trials without masking. This revealed a modulation of recurrent activity in the primary visual cortex rapidly after the onset of the feedforward sweep of processing in striate and extrastriate areas but significantly before the onset of attention-dependent recurrent modulations in V1. Our data provide direct support for the notion that (i) recurrent processing in V1 correlates with visual awareness and (ii) that attention and awareness involve distinct recurrent processing operations.

Fig. 1.

Stimulus setup. (a) Four small dots are placed around one search item; the dots designate the target and serve to mask it. In 67% of the trials the dots remain on screen after the search items disappear from screen (TM trials). In the remaining trials, search items and the dots disappear simultaneously (NTM trials). The small arrow indicates that search items in the lower quadrant are displaced away from the horizontal meridian to avoid potentially ambiguous magnetic field configurations (see Experimental Procedures). (b) Summary of the target duration individually adjusted for each subject (staircase procedure).

Fig. 2.

General waveforms/distributions and source localization results. (a) ERMF waveforms (total average across subjects) averaged across correct and incorrect TM trials at a central occipital (solid) and lateral occipitotemporal sensor site (dashed). The approximate location of the sensor sites are indicated by white and black circles in the distribution map. The arrowheads mark the onset of significant activity differences against baseline. Distribution maps at 80, 100, and 130 ms after search frame onset are shown on the right side. (b) Time course and distribution of sLORETA estimates of the total average response across subjects and conditions (correct TM trials). The red traces represent the time course of source activity at the source maximum in V1 (solid trace) and the left extrastriate cortex (dashed trace). (c) Time course and distribution of sLORETA estimates in a single subject.

Fig. 3.

Awareness related effects. (a) Average ERMF waveforms (black traces) for correct and incorrect TM trials of targets in the upper and lower VF. The gray areas highlight the time range of significant differences. The red traces illustrate the time course of source activity (estimates based on the correct-minus-incorrect difference of TM trials) at the calcarine fissure maxima for upper and lower VF targets (red arrows in b). (b and c) ERMF maps and sLORETA estimates of the correct-minus-incorrect difference for TM trials in the upper and lower VF at 110 ms. The total average across subjects and the single subject are shown in b and c, respectively. The small circle in b marks the sensor position from which the waveforms in a were recorded. The dashed line in c marks the localization of the calcarine fissure. (d) Illustration of the cruciform model. The horizontal meridian is slightly displaced toward the lower bank of the calcarine fissure (red arrow; see Experimental Procedures for details).

Fig. 4.

Attention-related effects. (a) Average ERMF waveforms (blue traces) elicited by correct TM trials of targets in the upper and the lower VF. The red trace represents the time course of source activity (estimates of the lower-minus-upper VF difference) at the calcarine maximum (red arrow in b). (b) ERMF distribution of the lower-minus-upper VF difference and corresponding sLORETA estimates at 280 ms. The small circle marks the location of the sensor site where the waveforms in a were recorded. (c) Illustration of the timing of frame B and mask D relative to the onset of the feedforward-driven activity in V1 A, the time range of significant awareness-related (orange) and attention-related (blue) activity. C marks the time point at which the frame-offset transient would arrive in V1 (frame duration of 85 ms plus 71 ms for the visual input to arrive in V1). (d) Control experiment. Percentage of correct target discriminations as a function of the subsequent awareness judgement of the observers.