Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection

Abstract

Covertly directing visual attention toward a spatial location in the absence of visual stimulation enhances future visual processing at the attended position. The neuronal correlates of these attention shifts involve modulation of neuronal "baseline" activity in early visual areas, presumably through top-down control from higher-order attentional systems. We used electroencephalography to study the largely unknown relationship between these neuronal modulations and behavioral outcome in an attention orienting paradigm. Covert visuospatial attention shifts to either a left or right peripheral position in the absence of visual stimulation resulted in differential modulations of oscillatory alpha-band (8-14 Hz) activity over left versus right posterior sites. These changes were driven by varying degrees of alpha-decreases being maximal contralateral to the attended position. When expressed as a lateralization index, these alpha-changes differed significantly between attention conditions, with negative values (alpha_right < alpha_left) indexing leftward and more positive values (alpha_left < or = alpha_right) indexing rightward attention. Moreover, this index appeared deterministic for processing of forthcoming visual targets. Collapsed over trials, there was an advantage for left target processing in accordance with an overall negative bias in alpha-index values. Across trials, left targets were detected most rapidly when preceded by negative index values. Detection of right targets was fastest in trials with most positive values. Our data indicate that collateral modulations of posterior alpha-activity, the momentary bias of visuospatial attention, and imminent visual processing are linked. They suggest that the momentary direction of attention, predicting spatial biases in imminent visual processing, can be estimated from a lateralization index of posterior alpha-activity.

Figure 1.

Experimental paradigm and sequence of events during each trial. A central fixation cross and two lateralized gray squares serving as position markers for visuospatial attention orienting were continuously displayed. Each trial was initiated by an auditory warning signal (white noise) of variable length. This was followed by a brief (50 ms) auditory cue instructing subjects to covertly direct their attention either to the left (100 Hz tone) or to the right (800 Hz tone) position marker. After a delay of 2560 ms, a target appeared for 40 ms either in the left or right gray square. Targets were more likely to appear at cued positions (p = 0.66). Subjects were asked to respond to a perceived target by a right-hand button press.

Figure 2.

Time course of grand-averaged α-band oscillatory activity as a function of cueing condition shown (A) for all recorded electrodes, and (B) for selected posterior electrode sites (pooled per hemisphere) that showed maximal modulation of α-band activity in the cue–target interval (left and right panels). The middle panel in B represents the time course of the corresponding α-lateralization index over the posterior recording sites. Sustained changes in α-band oscillations are seen in the cue–target interval (A, B, left and right panels), which depended on the cued direction of attention and the side of recording. These attention-related changes were driven by varying degrees of α decreases, being maximal over the hemisphere contralateral to the attended position and significantly different from baseline (precue period). The corresponding α-lateralization indices (B, middle) revealed an overall (negative) bias in the distribution of attention-related α activity (α_right < α_left), suggestive of an overall asymmetric attention bias (in favor of the left hemifield).

Figure 3.

Lateralization index of posterior α (left vs right hemisphere) versus behavioral lateralization index for target processing (left vs right hemifield). The leftmost boxes show the evolution of α-lateralization indices over precue and cue–target intervals (collapsed into 3 time windows). The rightmost boxes illustrate the corresponding left-right bias in target processing (in terms of either RT or DR). For both cueing conditions (light vs dark gray boxes), the α-lateralization index close to target onset (second half of cue–target interval) perfectly matches the left-right bias estimated from the behavioral responses to these targets. Note the different scaling for α and behavioral lateralization indices (left vs right y-axis). Whiskers indicate SE.

Figure 4.

Trial-by-trial variability in pretarget α index versus behavior. A, Average detection rates of left and right targets (±SE). B, Average reaction times to left and right targets (±SE). C, Distribution of left and right cue trials (mean ± SE) are displayed as a function of α-lateralization index before target onset (collapsed over second half of the cue–target interval), subdivided in five index groups. Each index group comprises data of at least 30 trials from each of the 10 subjects. The α-lateralization index is related to reaction time (B) but not detection rate (A) of forthcoming targets. Note the overall advantage for detection of left compared with right targets, both in terms of detection rates and reaction times, which might be attributable to “pseudoneglect,” the natural tendency of neurologically normal subjects to attend more easily to the left than to the right visual hemifield (see Results, Behavior: overall asymmetry in left versus right visual field processing). neg, Negative; pos, positive.