Søren K. Andersen

Feature-selective attention enhances color signals in early visual areas of the human brain

We used an electrophysiological measure of selective stimulus processing (the steady-state visual evoked potential, SSVEP) to investigate feature-specific attention to color cues. Subjects viewed a display consisting of spatially intermingled red and blue dots that continually shifted their positions at random. The red and blue dots flickered at different frequencies and thereby elicited distinguishable SSVEP signals in the visual cortex. Paying attention selectively to either the red or blue dot population produced an enhanced amplitude of its frequency-tagged SSVEP, which was localized by source modeling to early levels of the visual cortex. A control experiment showed that this selection was based on color rather than flicker frequency cues. This signal amplification of attended color items provides an empirical basis for the rapid identification of feature conjunctions during visual search, as proposed by “guided search” models.

Behavioral performance follows the time course of neural facilitation and suppression during cued shifts of feature-selective attention.

A central question in the field of attention is whether visual processing is a strictly limited resource, which must be allocated by selective attention. If this were the case, attentional enhancement of one stimulus should invariably lead to suppression of unattended distracter stimuli. Here we examine voluntary cued shifts of feature-selective attention to either one of two superimposed red or blue random dot kinematograms (RDKs) to test whether such a reciprocal relationship between enhancement of an attended and suppression of an unattended stimulus can be observed. The steady-state visual evoked potential (SSVEP), an oscillatory brain response elicited by the flickering RDKs, was measured in human EEG. Supporting limited resources, we observed both an enhancement of the attended and a suppression of the unattended RDK, but this observed reciprocity did not occur concurrently: enhancement of the attended RDK started at 220 ms after cue onset and preceded suppression of the unattended RDK by about 130 ms. Furthermore, we found that behavior was significantly correlated with the SSVEP time course of a measure of selectivity (attended minus unattended) but not with a measure of total activity (attended plus unattended). The significant deviations from a temporally synchronized reciprocity between enhancement and suppression suggest that the enhancement of the attended stimulus may cause the suppression of the unattended stimulus in the present experiment.

Effects of feature-selective and spatial attention at different stages of visual processing

We investigated mechanisms of concurrent attentional selection of location and color using electrophysiological measures in human subjects. Two completely overlapping random dot kinematograms (RDKs) of two different colors were presented on either side of a central fixation cross. On each trial, participants attended one of these four RDKs, defined by its specific combination of color and location, in order to detect coherent motion targets. Sustained attentional selection while monitoring for targets was measured by means of steady-state visual evoked potentials (SSVEPs) elicited by the frequency-tagged RDKs. Attentional selection of transient targets and distractors was assessed by behavioral responses and by recording event-related potentials to these stimuli. Spatial attention and attention to color had independent and largely additive effects on the amplitudes of SSVEPs elicited in early visual areas. In contrast, behavioral false alarms and feature-selective modulation of P3 amplitudes to targets and distractors were limited to the attended location. These results suggest that feature-selective attention produces an early, global facilitation of stimuli having the attended feature throughout the visual field, whereas the discrimination of target events takes place at a later stage of processing that is only applied to stimuli at the attended position.

Color-selective attention need not be mediated by spatial attention

It is well-established that attention can select stimuli for preferential processing on the basis of non-spatial features such as color, orientation, or direction of motion. Evidence is mixed, however, as to whether feature-selective attention acts by increasing the signal strength of to-be-attended features irrespective of their spatial locations or whether it acts by guiding the spotlight of spatial attention to locations containing the relevant feature. To address this question, we designed a task in which feature-selective attention could not be mediated by spatial selection. Participants observed a display of intermingled dots of two colors, which rapidly and unpredictably changed positions, with the task of detecting brief intervals of reduced luminance of 20% of the dots of one or the other color. Both behavioral indices and electrophysiological measures of steady-state visual evoked potentials showed selectively enhanced processing of the attended-color items. The results demonstrate that feature-selective attention produces a sensory gain enhancement at early levels of the visual cortex that occurs without mediation by spatial attention.

Neural mechanisms of intermodal sustained selective attention with concurrently presented auditory and visual stimuli

We investigated intermodal attention effects on the auditory steady-state response (ASSR) and the steady-state visual evoked potential (SSVEP). For this purpose, 40-Hz amplitude-modulated tones and a stream of flickering (7.5 Hz) random letters were presented concurrently. By means of an auditory or visual target detection task, participants’ attention was directed to the respective modality for several seconds. Attention to the auditory stream led to a significant enhancement of the ASSR compared to when the visual stream was attended. This attentional modulation was located mainly in the right superior temporal gyrus. Vice versa, attention to the visual stream especially increased the second harmonic response of the SSVEP. This modulation was focused in the inferior occipital and lateral occipitotemporal gyrus of both hemispheres. To the best of our knowledge, this is the first demonstration of amplitude modulation of the ASSR and the SSVEP by intermodal sustained attention. Our results open a new avenue of research to understand the basic neural mechanisms of intermodal attention in the human brain.

Attentional bias of competitive interactions in neuronal networks of early visual processing in the human brain

Multiple objects in a visual scene compete for neuronal representation. We investigated competitive neuronal dynamics in cortical networks of early visual processing in the human brain. Coloured picture streams flickered at 7.42 Hz, evoking the steady-state visual evoked potential (SSVEP), an electrophysiological response of neuronal populations in early visual areas synchronised by the external pacemaker. While these picture streams were at a fixed location in the upper left and right quadrant, respectively, additional competing picture streams flickering at a different frequency were continuously changing the distance to the stationary streams by slow motion. Analysis of the 7.42 Hz SSVEP amplitude revealed significant amplitude decreases when the competing stimulus was closer than about 4.5 degrees of visual angle. Sources of the SSVEP suppression effect were found in early visual areas of the ventral and dorsal processing streams. Attending the stationary stimulus resulted in no difference in 7.42 Hz SSVEP amplitude regardless of spatial separation to the competing stimulus. Contrary to the predictions of the model, we found co-amplification of the competing stimulus at close spatial proximity accompanied by an increase of an intermodulation frequency, suggesting integrated neuronal processing of target and competing stimuli when both streams are close together.

Time course of affective bias in visual attention: convergent evidence from steady-state visual evoked potentials and behavioral data.

Selective attention to a primary task can be biased by the occurrence of emotional distractors that involuntary attract attention due to their intrinsic stimulus significance. What is largely unknown is the time course and magnitude of competitive interactions between a to-be-attended foreground task and emotional distractors. We used pleasant, unpleasant and neutral pictures from the International Affective Picture System (IAPS) that were either presented in intact or phase-scrambled form. Pictures were superimposed by a flickering display of moving random dots, which constituted the primary task and enabled us to record steady-state visual evoked potentials (SSVEPs) as a continuous measure of attentional resource allocation directed to the task. Subjects were required to attend to the dots and to detect short intervals of coherent motion while ignoring the background pictures. We found that pleasant and unpleasant relative to neutral pictures more strongly influenced task-related processing as reflected in a significant decrease in SSVEP amplitudes and target detection rates, both covering a time window of several hundred milliseconds. Strikingly, the effect of semantic relative to phase-scrambled pictures on task-related activity was much larger, emerged earlier and lasted longer in time compared to the specific effect of emotion. The observed differences in size and duration of time courses of semantic and emotional picture processing strengthen the assumption of separate functional mechanisms for both processes rather than a general boosting of neural activity in favor of emotional stimulus processing.

Sustained Multifocal Attentional Enhancement of Stimulus Processing in Early Visual Areas Predicts Tracking Performance

Keeping track of multiple moving objects is an essential ability of visual perception. However, the mechanisms underlying this ability are not well understood. We instructed human observers to track five or seven independent randomly moving target objects amid identical nontargets and recorded steady-state visual evoked potentials (SSVEPs) elicited by these stimuli. Visual processing of moving targets, as assessed by SSVEP amplitudes, was continuously facilitated relative to the processing of identical but irrelevant nontargets. The cortical sources of this enhancement were located to areas including early visual cortex V1–V3 and motion-sensitive area MT, suggesting that the sustained multifocal attentional enhancement during multiple object tracking already operates at hierarchically early stages of visual processing. Consistent with this interpretation, the magnitude of attentional facilitation during tracking in a single trial predicted the speed of target identification at the end of the trial. Together, these findings demonstrate that attention can flexibly and dynamically facilitate the processing of multiple independent object locations in early visual areas and thereby allow for tracking of these objects.

Independent Effects of Attentional Gain Control and Competitive Interactions on Visual Stimulus Processing

Attention filters behaviorally relevant stimuli from the constant stream of sensory information comprising our environment. Research into underlying neural mechanisms in humans suggests that visual attention biases mutual suppression between stimuli resulting from competition for limited processing resources. As a consequence, processing of an attended stimulus is facilitated. This account makes 2 assumptions: 1) An attended stimulus is released from mutual suppression with competing stimuli and 2) an attended stimulus experiences greater gain in the presence of competing stimuli than when it is presented alone. Here, we tested these assumptions by recording frequency-tagged potentials elicited in early visual cortex that index stimulus-specific processing. We contrasted the processing of a given stimulus when its location was attended or unattended and in the presence or the absence of a nearby competing stimulus. At variance with previous findings, competition similarly suppressed processing of attended and unattended stimuli. Moreover, the magnitude of attentional gain was comparable in the presence or the absence of competing stimuli. We conclude that visuospatial selective attention does not directly modulate mutual suppression between stimuli but instead acts as a signal gain, which biases processing toward attended stimuli independent of competition.

Attentional Bias to Briefly Presented Emotional Distractors Follows a Slow Time Course in Visual Cortex

A central controversy in the field of attention is how the brain deals with emotional distractors and to what extent they capture attentional processing resources reflexively due to their inherent significance for guidance of adaptive behavior and survival. Especially, the time course of competitive interactions in early visual areas and whether masking of briefly presented emotional stimuli can inhibit biasing of processing resources in these areas is currently unknown. We recorded frequency-tagged potentials evoked by a flickering target detection task in the foreground of briefly presented emotional or neutral pictures that were followed by a mask in human subjects. We observed greater competition for processing resources in early visual cortical areas with shortly presented emotional relative to neutral pictures ∼275 ms after picture offset. This was paralleled by a reduction of target detection rates in trials with emotional pictures ∼400 ms after picture offset. Our finding that briefly presented emotional distractors are able to bias attention well after their offset provides evidence for a rather slow feedback or reentrant neural competition mechanism for emotional distractors that continues after the offset of the emotional stimulus.