Spatial attention modulates initial afferent activity in human primary visual cortex

Abstract

It is well established that spatially directed attention enhances visual perceptual processing. However, the earliest level at which processing can be affected remains unknown. To date, there has been no report of modulation of the earliest visual event-related potential component "C1" in humans, which indexes initial afference in primary visual cortex (V1). Thus it has been suggested that initial V1 activity is impenetrable, and that the earliest modulations occur in extrastriate cortex. However, the C1 is highly variable across individuals, to the extent that uniform measurement across a group may poorly reflect the dynamics of V1 activity. In the present study we employed an individualized mapping procedure to control for such variability. Parameters for optimal C1 measurement were determined in an independent, preliminary "probe" session and later applied in a follow-up session involving a spatial cueing task. In the spatial task, subjects were cued on each trial to direct attention toward 1 of 2 locations in anticipation of an imperative Gabor stimulus and were required to detect a region of lower luminance appearing within the Gabor pattern 30% of the time at the cued location only. Our data show robust spatial attentional enhancement of the C1, beginning as early as its point of onset (57 ms). Source analysis of the attentional modulations points to generation in striate cortex. This finding demonstrates that at the very moment that visual information first arrives in cortex, it is already being shaped by the brain's attentional biases.

Figure 1.

Probe task and procedure carried out in the preliminary session, independent of spatially directed attention. Data from a single subject (S#6) are shown. (a) Gabor stimuli were presented to 8 locations in a randomized sequence. Based on the resulting waveforms, we identified the pair of diagonally opposite locations from which the highest amplitude response within the C1 interval (50–80 ms) was elicited. (b) For these optimal locations, the negative and positive foci were identified in the scalp topography in the same C1 time frame for upper- and lower-field locations, respectively. (c) Average-reference waveforms were extracted from electrodes lying at the center of these foci.

Figure 2.

Spatial cueing task of the second session, incorporating the optimal pair of locations determined in session 1. (a) standard Gabor stimulus and target stimulus at difficulty level 7. (b) Task structure. In this example an invalid (uncued) target is presented, which is to be ignored.

Figure 3.

(a) Grand average waveforms for attention toward and away from upper- and lower-field stimuli. (b) P-values derived from running t-tests to determine the onset of the probe C1 from session 1 and the onset of the attention effect in session 2.

Figure 4.

Individual subject scalp topographies at the 80-ms time point for upper-field locations and at 80 and 100 ms for lower-field locations from the probe data, and attended and unattended waveforms (average reference) from the attention task data for the pair of diagonally opposite locations selected for each individual. Scalp electrodes selected to measure individual C1s on the basis of probe topographies are shown as green circles. C1 (80 ms) and P1 (100 ms) topographies for lower-field locations are shown on the same scale for each subject to highlight changes in amplitude as well as topographical focus.

Figure 5.

Average gaze deviations for trials accepted to the ERP analysis, superimposed on the stimulus display. Both upper and lower locations are shown for each subject in different colors. The stimulus is a level 7 target.