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Accurate perception of stimuli that appear in the visual fields maybe achieved by covertly directing attention to the stimulus locationswithout moving the eyes1,2. This ability to move attention volun-tarily has been likened metaphorically to a ‘spotlight’3 or ‘zoom lens’4

that can be shifted from one location to another while examining avisual scene. Psychophysical studies have shown that stimuli at anattended location are detected and discriminated more accuratelyand responded to more rapidly than are stimuli at an unattendedlocation3–6.

The speed with which attention can be shifted from one stimu-lus location to another depends on a number of factors, most impor-tantly the salience, discriminability and positioning of theattention-directing cues7. When an attentional shift is triggered by asymbolic cue, such as an arrow pointing to a relevant location, thetime required to disengage attention from the cue’s location andfully re-engage it at the new location designated by the cue has beenestimated at 300-600 ms based on behavioral studies7–10. A similarattentional switching time has been reported in situations wheresubjects had to identify two targets in rapid succession at the samelocation11–13. A number of time-dependent processes have beenproposed to carry out the switching of visual-spatial attention fromone location to another, including discriminative processing of thecue information8, disengagement, movement and re-engagementof the attentional focus1, build-up of sensory facilitation in the visu-al pathways corresponding to the new location14 and gating (entry)of the new information into short-term memory for conscious per-ception15. It has proven difficult, however, using behavioral mea-sures alone, to study the respective time courses of these componentprocesses of attentional switching.

The present study used an electrophysiological measure of sen-sory facilitation in the visual cortical pathways in conjunction withbehavioral data to examine the temporal dynamics of attentionalswitching. In both animals16–18 and humans19,20, transient stim-ulus-evoked neural activity in extrastriate visual cortex is enhancedwhen attention is directed toward (versus away from) the location

of the evoking stimuli. These attention-related changes in corticalresponse aptitudes have been attributed to a sensory gain-controlmechanism that amplifies visual inputs coming from attendedlocations21. Current evidence indicates that this sensory facilita-tion takes place at the level of extrastriate visual cortex rather thanin primary visual cortex19.

This facilitation of attended inputs can also be measured inhumans by recording the steady-state visual evoked potential(SSVEP) elicited in extrastriate cortex by rapidly flickering stim-uli22–24. The SSVEP has a sinusoidal waveform at the frequencyof the flickering stimulus and is substantially increased in ampli-tude when attention is focused upon the location of the stimulus.The SSVEP has advantages over the transient evoked potentialas a measure of relative attention, because it is a robust oscillat-ing signal that can be extracted rapidly from the ongoing elec-tro-encephalogram (EEG) using frequency-domain analysismethods25. Most importantly, the SSVEP is an ongoing wave-form that indexes attention-related changes in cortical facilita-tion continuously rather than intermittently as with transientevoked potentials. By studying the time course of SSVEP ampli-tude changes following an attention-directing cue, we estimat-ed the speed with which newly attended inputs are facilitated inthe visual cortex during attentional switching.

ResultsInformed consent was obtained from nine subjects who viewed astimulus display of light-emitting diodes (LEDs) while brain elec-trical activity was recorded non-invasively from 30 scalp electrodesmounted in an elastic cap. The display contained two vertical rowsof five LEDs each, situated five degrees to the left and right of a cen-tral fixation point (Fig. 1). Each trial began with the simultaneousonset of flickering of both rows of LEDs; all LEDs in the left rowflickered synchronously at 20.8 Hz and those in the right row at 27.8Hz. A centrally located cue appeared to the left or right of the fixa-tion point 1.3 seconds after the onset of flicker; this cue directed the

articles

The time course of cortical facilitation during cued shifts of spatial attention

Matthias M. Müller1, Wolfgang Teder-Sälejärvi2 and Steven A. Hillyard2

1 Department of Psychology, University of Konstanz; Fach D25, D-78457 Konstanz, Germany2 Department of Neurosciences, University of California at San Diego, 9500 Gilman Drive, La Jolla, California 92093-0608, USA

Correspondence should be addressed to M.M.M. (matthias.m.mueller@uni-konstanz.de)

Adaptive behavior requires the rapid switching of attention among potentially relevant stimuli thatappear in the environment. The present study used an electrophysiological approach tocontinuously measure the time course of visual pathway facilitation in human subjects as attentionwas shifted from one location to another. Steady-state visual evoked potentials (SSVEPs) wererecorded to rapidly flickering lights at attended and unattended locations, and variations in SSVEPamplitude over time were calculated after a cue to shift attention. The build-up of corticalfacilitation reflected in SSVEP amplitude was found to bear a close temporal relationship with theemergence of accurate target discriminations at the newly attended location.

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632 nature neuroscience • volume 1 no 7 • november 1998

subject to shift attention to the flickering row of LEDs on the sameside and to report occurrences of color-change targets in that rowby pressing a button. Targets occurred unpredictably throughoutthe 3.0-second interval of continuous flickering following the cue.

As in our previous study18, the most pronounced SSVEP atten-tion effects were found at occipito-temporal scalp sites (contralat-eral to the visual field of stimulation; Fig. 1). The SSVEP amplitudesto the left and right stimuli were measured in the frequency domainby fast-Fourier transform (FFTs) at the respective flicker frequen-cies. The analysis windows for the FFT (480 ms in duration for leftstimulus; 360 ms for right stimulus) were moved progressively alongthe averaged SSVEP waveform (Fig. 2a) to produce a continuousfunction of SSVEP amplitude change over time (Fig. 2b). Mainte-nance of central eye fixation was verified by recordings of the elec-trooculogram, and trials contaminated with eye movements, blinksor other artifacts were rejected from analysis.

The time course of SSVEP amplitude changes following the cueto shift attention was averaged across all nine subjects for the leftstimulus (Fig. 3a) and for the right stimulus (Fig. 3b). For eachstimulus, the SSVEP curves are superimposed for the attended andunattended conditions, as determined by the direction of the cue.The SSVEP elicited by the attended flickering row showed a sharpincrease in amplitude from baseline starting at around 100–200 msafter the cue. This increase became significantly greater than base-line during the interval 240–288 ms after the cue for the right rowand 288–336 ms for the left row (both p < 0.05). The midpoints ofthese intervals are indicated by vertical lines in Fig. 3. In contrast,the SSVEP to the same stimuli when unattended showed no sig-nificant deviations from baseline. The SSVEP to the attended stim-ulus remained significantly greater than to the unattended stimulusfor the remainder of the trial.

Target-detection rates also showed a steep increase as a func-tion of time after the cue (Fig. 3, bar graphs). For both the left andright stimuli, there were significant increments in correct targetdetections during the second 144-ms interval following the cue rel-ative to the first interval (p < .01), during the third interval relativeto the second (p < .01) and during the fourth interval relative tothe third (p < .02). From the fourth interval (432–576 ms) onwards,behavioral detection rates remained stable. Individual subjects dif-fered considerably, however, in how rapidly their detection perfor-mance reached asymptotic levels. Dividing the subjects into the

four fastest and four slowest individuals on this behavioral mea-sure revealed strongly correlated changes in the rise time of SSVEPamplitude (Fig. 4). The fast switchers reached their peaks of SSVEPamplitude significantly earlier than the slow switchers, by 195 msfor left-field stimuli and by 269 ms for right-field stimuli (both p< .05). The correlation of SSVEP peak latency and the time bin ofasymptotic detection performance over the first 600 ms followingthe cue was highly significant for both left (r = 0.78, p < .01) andright (r = 0.80, p < .01) stimuli.

articles

Fig. 1. Schematic diagram of stimulus array and electrodepositions, with SSVEP waveforms from one subject shownfor the attended (boldline) and unattended (thin line) con-ditions recorded from contralateral occipito-temporalsites TO2 and TO1. The flicker rates were 20.8 Hz for theleft row and 27.8 Hz for the right row of LEDs. The fourpossible color configurations are shown for each row,with all five LEDs being red in the standard configuration.Target and non-target color changes (two LEDs changedto green) occurred in random order on both sides with astimulus-onset asynchrony of 400 to 700 ms (onset toonset). Gray oval is the fixation point. The SSVEPs wereobtained by a sliding average technique in the timedomain16–18 and were time-locked to either the left or theright flickering stimulus.

Fig. 2. Representative time- and frequency-domain waveformsfrom a single subject. (a) Averaged time-domain waveform follow-ing the cue to attend right and time-locked to the right flickeringstimulus. SSVEP activity to this attended flicker can be seen at theexpanded time scale. (b) Time course of SSVEP amplitude in thefrequency domain obtained from the waveform shown in (a) by amoving-window Fast Fourier Transform (FFT) at the stimulus fre-quency; successive window steps were 4 ms. Thin horizontal line isdrawn through pre-cue baseline. Bold tracing is attended waveform;thin tracing shows unattended waveform elicited by the same stim-ulus. Note that the last 500 ms were not analyzed because the mov-ing window reaches the end of the epoch.

a

b

Expanded time scale for attend right condition

Cue

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nature neuroscience • volume 1 no 7 • november 1998 633

DiscussionThe average time required to reach asymptotic levels of target detec-tion performance after cue onset (432–576 ms) corresponds wellwith previous estimates of attentional switching time for endoge-nous cues7 and the attentional ‘dwell time’ for rapid sequential dis-criminations8,13. To compare these behavioral findings with the timecourse of cortical facilitation, we must take into account that theSSVEP amplitude curves were calculated in the frequency domainwithin moving windows that extended 360 ms (for right stimuli) or480 ms (for left stimuli) in advance of the plotted values. Accord-ingly, the abrupt, monotonic increases in the windowed SSVEP func-tions starting at 100–200 ms post-cue (Fig. 3) reflect the leadingedges of the moving windows encountering the initial amplitudeincreases in the raw SSVEP waveforms having a latency some 360or 480 ms longer. In other words, these windowed functions repre-sent increments in SSVEP magnitude that were delayed by anamount equivalent to the window duration but were well localizedin time. The initial significant increases in windowed SSVEP ampli-tude at 240–336 ms after the cue thus represent enhanced evokedneural activity in the visual cortex during the latency range 600–800ms after the attention-directing cue.

To relate this cortical facilitation to the time course of target detec-tion accuracy, we must also factor in the time delay between stim-ulus delivery and the evoked cortical activity that is facilitated byattention. The SSVEP facilitation is localized to extrastriate visualcortex of the occipital lobe22,24, and this enhanced neural activityhas a post-stimulus latency of 100–150 ms19,20. Thus, the initialincrease of SSVEP amplitude at 600–800 ms represents the enhance-ment of cortical activity elicited by attended stimuli delivered100–150 ms earlier, that is, during the interval 450–650 ms after thecue, at which time detection performance was reaching its maxi-mum. These findings suggest that optimal perception of the newlyattended target stimuli depends upon the facilitation of the corticalevoked activity representing those stimuli.

The 600–800 ms delay observed between cue onset and thefacilitation of attended inputs in the cortex reinforces the con-clusion13 that “visual attention is not a high speed switchingmechanism.” In the present design, this delay included the timerequired to discriminate the direction of the attention-directingcue, which was situated 0.4 degrees to the left or right of fixa-tion. Although this cue was thus slightly lateralized to the attend-ed side, it was more akin to an endogenous, central-arrow cue

than to an exogenous (peripheral) cue occurring atthe to-be-attended location, which presumablywould have triggered a much faster and more auto-matic switching of attention1,7.

The present SSVEP recordings provide a continu-ous measure of the time course of an essential compo-nent of attentional switching, namely the facilitation ofevoked activity in the visual-cortical pathways inresponse to the newly attended stimulus. Our analysisshows that the timing of this facilitation correspondswell with attaining maximal target detection perfor-mance, and the temporal correspondence between theseelectrophysiological and behavioral measures was rein-forced by significant inter-individual correlations.Moreover, the effect of switching attention from thecentral cue to a lateral flickering stimulus was found tobe purely facilitatory, with no significant inhibition ofthe SSVEP to the unattended-location stimuli in theopposite visual field. We propose that this facilitationrepresents the operation of a sensory gain-controlmechanism that enhances the signal-to-noise ratio and

articles

Fig. 4. Time course of SSVEP amplitude increases (moving window FFT functions)and percentage of correct target detections (with standard errors) in 144-ms binsplotted separately for the four subjects who showed the fastest switching ofattention following the cue (bold line, open bars) and the four subjects showingthe slowest switching time (thin line, solid bars). The time bin for which subjectsreached their maximum performance was correlated with the latency of the peakof the SSVEP amplitude. (a) left stimulus, (b) right stimulus.

Fig. 3. Electrophysiological and behavioralindices of attentional switching. Upperpanel, time course of baseline-correctedSSVEP amplitude (moving window FFT func-tions) for the attended (bold) and unat-tended (thin line) conditions averagedacross all subjects for left (a) and right (b)visual-field stimuli. Recordings are fromcontralateral occipitotemporal sites TO2(left hemifield stimulation) and TO1 (righthemifield stimulation). The vertical line rep-resents the midpoint of the first 48-ms timebin having a statistically significant differencebetween baseline and post-cue SSVEPamplitude for the attended condition.Lower panel, mean percentage of correcttarget detections (with standard errors) in17 successive 144-ms bins for the left (a)and right (b) bar averaged across all subjects.

a bLeft stimulus Right stimulus

Percentcorrecttarget

detections

Cue onset Cue onset

a bLeft stimulus Right stimulus

Cue onset Cue onset

Percent correcttarget detectionsfor fast (white)

and slow (black)switchers

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634 nature neuroscience • volume 1 no 7 • november 1998

hence the discriminability of attended-location stimuli21. Currentevidence indicates that this gain control takes place in extrastriatevisual cortex19,22,24 and is regulated by a network of cortical and sub-cortical structures, including prefrontal and posterior parietal areasand the pulvinar of the thalamus5,26. The use of on-line electro-physiological measures of sensory processing is a useful adjunct tobehavioral measures for analyzing the timing of attentional switch-ing and selection processes27,28.

MethodsThe two LED rows subtended a viewing angle of 3.45 x 0.5 degrees each at aviewing distance of 58 cm. The on-off duty cycles were 50/50 for both fre-quencies, and the ‘on’ luminance was 7.5 cd/m2 against a background lumi-nance of 0.6 cd/m2. All LEDs began flickering in red, but at random intervalsof 400–700 ms (onset to onset) two of the LEDs in a row changed briefly(for 144 ms) to green (Fig. 1); color changes of LEDs at the top and bottomof the attended row were defined as targets. Targets and non-target colorchanges were presented in random order with equal probability for both leftand right stimuli. However, subjects only responded to the targets occurringon the attended side as directed by the lateralized cue.

The experiment consisted of 250 trials each for the attend-right andattend-left conditions, divided in 20 blocks of 25 trials each. To increase moti-vation, subjects received an additional reward of 50 cents for each block inwhich they detected at least 80% of the targets on the attended side. Theresponding hand was changed halfway through the experiment, and thesequence of hand usage was counterbalanced across subjects. The electrodepositions are shown schematically in Fig. 1, and their coordinates are givenin ref. 29. The EEG was recorded with a sample rate of 250 Hz and a band-pass of 0.3–100 Hz, except for the horizontal electro-oculogram (EOG)where the bandpass was 0.01–100 Hz. Individual trials were rejected fromfurther analysis on the basis of blink or EMG artifacts in the scalp channels,or when lateral eye movements monitored in the averaged horizontal EOGdeviated more than 0.5 degrees from fixation. The mean rejection rate was13.5% of attend-right trials and 13.9% of attend-left trials.

To ascertain the time course of SSVEP amplitude changes, artifact-freeEEG epochs were averaged separately following the attend-left or attend-right cues. The averaging epochs extended from 1000 ms before to 3000 msafter cue onset. A moving Blackman-Harris window FFT restricted to thefrequency of stimulation with a window length of ten cycles was applied to theaveraged SSVEP waveforms, resulting in window durations of 480 ms forthe left and 360 ms for the right stimulus. These window durations werechosen to eliminate crosstalk between the two frequencies to be analyzedand to ensure comparable signal-to-noise ratios in their respective analysiswindows. SSVEP amplitudes were calculated in microvolts as the square rootof the sum of the squared real and imaginary components for each successiveposition (in 4-ms steps) of the moving window. Baseline was defined asmean amplitude from 1000 to 500 ms before cue onset.

Mean SSVEP amplitudes were calculated for sequential 48-ms bins ofthe moving window FFT function over the first 432 ms after cue onset.These values were tested against baseline by means of paired t-tests todetermine the first bin that showed a significant amplitude increase rel-ative to baseline. For the remaining epoch, the mean SSVEP amplitudeswere calculated for 144-ms bins. Baseline-corrected mean amplitudechanges were tested by means of a three-factor, repeated-measuresANOVA (Electrode site-TO1/TO2 x Time Bin x Attention). In addition,the peak latencies of SSVEP amplitudes for fast and slow switchers werecompared by means of unpaired t-tests for left and right stimuli. Thepercentage of correct target detections was calculated for 144-ms timebins over a period beginning at cue-onset and extending to 2448 ms aftercue onset. This bin width corresponded to the144-ms durations of thetarget and non-target color changes, thereby ensuring an equal distrib-ution of these stimulus types across all of the time bins. The time bin forwhich subjects reached their maximum performance was correlated withthe latency of the peak of SSVEP amplitude.

AcknowledgementsWe thank Jon Hansen, Lourdes Anllo-Vento, Matt Marlow and Carlos Nava for

technical advice and support. The work was supported by grants from ONR

(N00014-93-I-0942), NIMH (MH-25594), NIH (NS 17778) and the Deutsche

Forschungsgemeinschaft.

RECEIVED 1 JULY: ACCEPTED 18 SEPTEMBER 1998

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