Hemispheric modulations of alpha-band power reflect the rightward shift in attention induced by enhanced attentional load

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Neuropsychologia 47 (2009) 41–49

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Hemispheric modulations of alpha-band power reflect the rightward shiftin attention induced by enhanced attentional load

Alejandro Péreza,∗, Polly V. Peersb, Mitchell Valdés-Sosaa, Lídice Galána,Lorna Garcíaa, Eduardo Martínez-Montesa

a Department of Cognitive Neurosciences, Cuban Neuroscience Center, Avenida 25 # 15202, Cubanacán, Playa, Ciudad Habana, Cubab MRC Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB 2 2EF, UK

a r t i c l e i n f o

Article history:Received 14 August 2007Received in revised form 13 August 2008Accepted 18 August 2008Available online 22 August 2008

Keywords:AttentionLateralizationTOJBias

a b s t r a c t

Rightward shifts in attention are a common consequence of brain injury. A growing body of evidenceappears to suggest that increases in attentional load, and decreases in alertness can lead to rightwardshifts in attention in healthy and patient populations. It is unclear however whether these factors affectspatial biases in attention at the level of preparatory control processes or at the level of stimulus drivenexpression mechanisms. Whilst such effects cannot easily be dissociated behaviourally, the robust asso-ciation between changes in �-band activity and shifts in visual attention provides a neural marker bywhich the temporal dynamics of effects of attentional load on spatial processing might be examined.Here we use electroencephalography to examine the relationship between modulations in �-band activ-ity and behavioural outcome on a dual task paradigm comprising a detection task (t1), closely followedby a temporal order judgment task (t2). We examine the effects of high (respond to t1 and t2) and low (t2only) attentional load conditions on spatial bias and changes in lateralization of �-band activity over thecourse of the trial. As anticipated a rightward bias in detecting target onsets was observed in the temporalorder judgment task (t2) under conditions of high attentional load. This rightward shift in attention wasassociated with changes in the lateralization of �-band activity that occurred only after the presentationof t2, suggesting that attentional load may primarily influence expression mechanisms.

© 2008 Elsevier Ltd. All rights reserved.

1. Introduction

An attentional bias, usually to the right side of visual space, is acommon consequence of right parietal brain damage, leading to thewidely investigated behavioural phenomena of unilateral neglect(Danckert & Ferber, 2005; Driver & Vuilleumier, 2001) and visualextinction (Baylis, Simon, Baylis, & Rorden, 2002; Vuilleumier &Rafal, 2000). A growing body of recent research appears to pointto an analogous rightward attentional bias in healthy individualsunder certain conditions. An example of this comes from Manlyand colleagues who found that reductions in vigilance resultingfrom sleep deprivation, or the length of time engaged in the task,was associated with a rightward shift on a line bisection task(Manly, Dobler, Dodds, & George, 2005). The authors argue thatthe changes in alertness observed in their fatigued healthy indi-viduals (and commonly seen in patients with unilateral neglect),

∗ Corresponding author at: Calle 1ra e/10 y 12 Edif # 637 Apto 63, Plaza de laRevolución, Ciudad de La Habana, CP 10 400, Cuba. Tel.: +53 7 8377678.

E-mail address: [email protected] (A. Pérez).

may directly influence spatial attention. In line with this notion,Bellgrove and colleagues have shown that healthy individuals whoperformed poorly on a sustained attention task showed a rela-tive rightward shift in attention, as measured by the GreyscalesTask, compared to those who performed well (Bellgrove, Dockree,Aimola, & Robertson, 2004). In both these studies the rightwardshift observed took the form of an attenuation of the normal left-ward spatial bias, known as pseudoneglect (Bowers & Heilman,1980), that is typically seen in healthy subjects on a broad rangeof spatial attention tasks (Luh, Rueckert, & Levy, 1991; Milner,Brechmann, & Pagliarini, 1992; Nicholls, Mattingley, & Bradshaw,2005). Taken together these results appear to suggest that sustainedattention may have a modulatory effect on spatial processing.

The temporal order judgement (TOJ) paradigm (Titchener, 1908)has frequently been used to assess spatial biases. The TOJ task mea-sures the relative speed of awareness for events occurring on theleft and right sides of space. This is achieved by manipulating therelative onsets of stimuli appearing to the left and right of fixation,and asking participant to report which target appeared first. Typ-ically, explicitly directing attention to one side of the visual fieldwith a spatial cue produces a bias to report stimuli presented on

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42 A. Pérez et al. / Neuropsychologia 47 (2009) 41–49

that side as appearing first (Schneider & Bavelier, 2003). Withoutspatial cues, neglect and extinction patients exhibit a systematicbias to report right-sided targets as appearing first (even when theleft stimulus onsets first) (Baylis et al., 2002; Di Pellegrino, Basso,& Frassinetti, 1997; Rorden, Mattingley, Karnath, & Driver, 1997).Surprisingly, this lateral bias is ameliorated by the introductionof occasional ‘alerting’ tones that are devoid of spatial informa-tion (Robertson, Mattingley, Rorden, & Driver, 1998), suggestingnon-spatial attentional processes influence spatial prioritization(Husain, 2005).

A recent study examined the effects of attentional load on spa-tial bias in healthy subjects using the TOJ task (Pérez, García, &Valdes-Sosa, 2008). A modification of the ‘attentional blink’ (AB)paradigm (Raymond, Shapiro, & Arnell, 1992), was used to manip-ulate attentional demands. In the AB paradigm two sequentiallypresented target stimuli (t1 and t2) have to be identified. Recog-nition of the second target (t2) is impaired, the ‘attentional blink’,when it is presented within a few hundred milliseconds of t1, butonly when the latter must be actively recognized (Duncan, Ward,& Shapiro, 1994; Raymond et al., 1992). Pérez and colleagues usedTOJ stimuli as the second target (t2) in the AB, and required par-ticipants to judge the order of left and right stimuli. They foundthat the reduction of attentional resources subsequent to t1 pro-cessing led to a rightward shift to the subsequent TOJ, eliminatingthe pseudoneglect observed in the focussed attention condition. Incontrast, the rightward shift was absent if t1 was ignored, a hall-mark of the AB distinguishing it from sensory masking. Importantly,the t1 stimulus had no spatial directionality (i.e. was uninformativeabout the order of the TOJ). The most parsimonious interpreta-tion of this result is that processing the central target stimulus (t1)reduces attentional resources and as a result induces a rightwardshift in attention. This study, along with other studies using differ-ent paradigms (Bartolomeo, 2000; Humphreys, Datar, Boucart, &Riddoch, 1996; Peers, Cusack, & Duncan, 2006), reinforces the ideaof a link between spatial bias and general cognitive resource, sug-gesting that a reduction of available processing resources can reveala right-lateralized bias of the residual capabilities.

Previous research has shown that �-band (∼8–14 Hz) activ-ity is a sensitive indicator of visual attentional shifts (Babiloniet al., 2004; Bastiaansen, Bocker, Brunia, de Munck, & Spekreijse,2001; Klimesch, Doppelmayr, Russegger, Pachinger, & Schwaiger,1998; Worden, Foxe, Wang, & Simpson, 2000). Decreased activityis observed at sites processing the attended side of space (Sausenget al., 2005; Thut, Nietzel, Brandt, & Pascual-Leone, 2006; Yamagishiet al., 2003) whilst corresponding increases are seen in regions pro-cessing the unattended side (Kelly, Lalor, Reilly, & Foxe, 2006; Rihs,Michel, & Thut, 2007; Worden et al., 2000; Yamagishi et al., 2003).In addition, alpha rhythm appears to be sensitive to attentionaldemands (Mulholland, 1969; Ray & Cole, 1985), with the durationof its desynchronization increasing with increased task complexity(Valdes-Sosa et al., 1994). Here, we build on previous EEG studiesof spatial cuing to explore the neural basis of the rightward bias ofresidual attention found in the AB paradigm (Pérez et al., 2008).

A currently unaddressed issue is at what stage in processingdoes the rightward attentional bias occur? Current neurophysiolog-ical models of attention make a distinction between two separatecomponents; control mechanisms and expression mechanisms(Gazzaniga, 1998; LaBerge, 1995; LaBerge, 2001). In this concep-tion, control mechanisms are involved in the allocation of attention,helping to select the objects or places to be attended on the basis ofbehavioural relevance. This mechanism precedes perception andoccurs during anticipation or preparation of an upcoming event(e.g. when an area of visual space is pre-cued as the likely locationof an upcoming stimulus). Regions of dorsolateral prefrontal andsuperior parietal cortex (Chafee & Goldman-Rakic, 2000; Corbetta,

Miezin, Shulman, & Petersen, 1993), as well as the anterior cin-gulate (Mesulam, Nobre, Kim, Parrish, & Gitelman, 2001; Posner& Petersen, 1990) appear to be implicated in this process. Fronto-parietal control mechanisms also bias activity in lower-level visualareas to prepare for upcoming visual processing, it is possible there-fore the alpha-correlate of attention shifts might originate in theseearlier visual areas.

In contrast, expression mechanisms reflect attentional compe-tition between stimuli, the means by which neural representationsof attended objects are boosted and representations of unattendeditems are suppressed by gain-control of the incoming visual signal(Desimone & Duncan, 1995; Duncan, Humphreys, & Ward, 1997).Anatomically these processes have been associated with effectswithin visual extrastriate cortex (Mangun, Buonocore, Girelli, & Jha,1998; Spitzer, Desimone, & Moran, 1988), with comparable findingsreported for both object based (Valdes-Sosa, Bobes, Rodriguez, &Pinilla, 1998) and location based (Mangun & Hillyard, 1990) selec-tion.

To examine the relative influences of expression and controlmechanisms in inducing a rightward shift in attention under con-ditions of high load we employed the same basic design used byPérez et al. (2008) whilst simultaneously taking EEG recordings.Changes of �-band spectral power were measured in healthy indi-viduals whilst they carrying out a TOJ task under conditions of highor low attentional load. We used an �-band lateralization index toassess whether rightward shifts in attention were associated withan asymmetry in oscillatory activity. To assess the relative contri-butions of expression and control mechanisms to rightward shiftsof attention we investigated whether differences in �-band powerlateralization index would occur both in anticipation of the t2 onsetand in the absence of t2 presentation, indicating an interaction ofattentional load with spatial processes at the level of anticipatoryattentional control, or alternatively whether lateralization effectsonly occur after t2 onsets, suggestive that such processes are morestimulus driven.

2. Methods

2.1. Participants

Twenty subjects (mean age 28, range 18–32 years, 13 males) were recruited tothe study, which was carried out in accordance with the principles laid down in theDeclaration of Helsinki. All subjects provided written informed consent. They wereall right handed as assessed by the Edinburgh Handedness Inventory (Oldfield, 1971)and had normal or corrected to normal visual acuity. They were in good health, hadno past history of psychiatric or neurological illness.

2.2. Instruments

The experiment was conducted in a quiet room with natural illumination. Stim-uli were presented on a 15′′ sVGA computer display with 800 × 600 pixels resolutionand a black background, controlled by a 933 MHz Intel Pentium III Copermine com-puter. The experiment was programmed using Cogent 2000 (Cogent 2000 team, FILand the ICN) and Cogent Graphics (John Romaya, Wellcome Department of ImagingNeuroscience) running on Matlab 6.5 (The MathWorks Inc.). The EEG recording wasperformed with a MEDICID 5 system (Neuronic SA, Havana).

2.3. Procedure

Participants were seated in a comfortable reclining chair at a distance of 50 cmfrom the screen. They were instructed to maintain fixation throughout the exper-iment on a diamond shape presented in the middle of the screen and to remainstill.

Each trial followed essentially the same pattern (Fig. 1). The trial, initiated by abutton press, commenced with the presentation of a white square (of 0.8◦) with ablack diamond in the centre of it, on an otherwise black screen. After a random delayranging from 500 to 800 ms, one of the four corners of the diamond disappeared for30 ms (t1).

The restored diamond shape was then shown for a further 280 ms (a delay likelyto produce a large AB) prior to the presentation of a target stimulus (t2) correspond-ing to a TOJ task. This t2 stimulus could initially appear as either a single circle, or

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Fig. 1. Experimental paradigm and sequence of events during each trial. A centralfixation shape was continuously displayed. After a random delay (500–800 ms), onecorner of the inner diamond (in this case the upper) disappeared for 30 ms (t1). Therestored corner was then shown for a further 280 ms prior to the onset of two circles(the t2 target). Circles onsets were jittered (�T), so the second would appear either120, 90 ms or at the same of the first (SOAs) (in case depicted left appears first). Thenboth remained on the screen for 400 ms before offset. After completion of 1180 msfrom the t1 presentation a warning tone prompted participants to respond.

two circles (in the case of simultaneous presentation in the TOJ), with 0.7◦ radiusand subtending 3.5◦ to the left or/and right of the fixation diamond. The stimulusonset asynchrony (SOA) of the two circles were jittered so that the left circle wouldappear either 120 or 90 ms before the right, at exactly the same time as the rightcircle, or 90 or 120 ms after the right circle, with an unequal number of trials in eachcondition. The circles then remained on the screen for 400 ms before offsetting atthe same time. The central shape remained on the screen at all times. A warningtone at the end of each trial (1180 ms after t1 was presented) prompted participantsto make their responses. Participants used arrow keys to indicate which of the fourcorners of the diamond had disappeared and to indicate whether they perceivedthe left or the right circle appearing on the screen first. Responses were given in thesame order that the target stimuli were presented.

Two separate blocks were completed. In one block responses to both t1 and t2were required, therefore provoking a high attentional load condition (H condition).In the other block subjects were only required to perform the TOJ and asked toignore t1. This was the low attentional load condition (L condition) block. In the Lcondition block the local shape-change was the same on all trials, and consisted ofthe disappearance and re-appearance of the upper corner. The order in which blockswere completed and the response hand were counterbalanced across participants.

In each block 400 trials were presented distributed as follows: 150 trials in whichthe t2 circles appeared simultaneously (double simultaneous stimulation), 100 trialsin which their onsets were asynchronous.1 In addition 150 ‘catch trials’ (t1 only) wereincluded in which the t2 did not appear despite expectations. These trials enabledus to monitor whether �-band asymmetries occurred in the absence of t2. Trialswere presented in a pseudorandom order. The experiment was preceded by a shorttraining period of 5–10 trials on each task to ensure that the participant had fullyunderstood the instructions.

2.4. EEG recording

Electrophysiological data was acquired using gold plated disk electrodes fromfourteen channels (P3, P4, O1, O2, T3, T4, T5, T6, C3, C4, F3, F4, F7 and F8) placedaccording to the International 10–20 system. All electrodes were referenced to anelectrode placed on the tip of the nose. The impedance of all electrodes was keptbelow 5 k�. Four additional electrodes used to record horizontal and vertical eyemovements (EOG) were located above and beneath the right eye and on the lateralorbital ridges of both eyes. The signals were amplified by a factor of 1000 and filteredbetween 0.05 and 30 Hz. EEG was continuously recorded (sampling rate 200 Hz).Epochs beginning 400 ms prior to the onset of t1 and continuing for 1100 ms were

1 Distributed evenly across the four possible onset asynchronies.

created. Artifact rejection was based on a threshold of 60 �V and trials contain-ing eyes movements (∼2◦) were also rejected. In addition, each EEG segment wasvisually inspected and those epochs with generalized artifacts were manually elim-inated. After rejections a total of 5373 trials were analyzed in trials with both t1 andt2; and 5018 in trials with only t1. The average number of trials suitable for analysisper person was 520, with the person with the greatest number of rejected trials stillhaving 356 analysable trials.

2.5. Electrophysiological analysis

For each EEG-epoch the event related potential (ERP) was subtracted (Mulleret al., 1996; Priestley, 1988). Then, time-varying power spectra of each trial wereobtained by means of Morlet wavelet analysis (Bertrand & Pantev, 1994; Tallon-Baudry & Bertrand, 1999) for each participant, experimental condition and channelin the frequency range from 1 to 30 Hz with step size of 0.5 Hz. The complex Mor-let wavelets were set to the selected constant ratio of 7 in order to have a goodcompromise between time and frequency resolution (Gruber, Muller, Keil, & Elbert,1999; Tallon-Baudry, 2004). The power spectra were averaged across trials to obtainthe mean spectral power (MSP), which was divided by the MSP in the pre-stimulusperiod (excluding the 50 ms before t1 onset) for baseline correction. The individ-ual baseline-corrected MSPs were averaged in the individual alpha frequency range(IAF) (mean = 11.25, S.D. = ±2.34) of each individual. This was defined as a frequencyrange of ±2 Hz centred around the individual frequency peak within the �-band(8–12 Hz), obtained from occipital electrodes in baseline period (see Thut et al., 2006for a similar procedure). The IAF accounts for inter-individual differences (Thut etal., 2006) and minimises interactions with other frequency bands, particularly thetheta band (Klimesch et al., 1998). Subsequent analyses were carried out in a timewindow ranging from −200 to 1000 ms (t1 at 0 ms), to obtain data consisting of one�-band MSP time series (240 time samples) for each electrode (14 channels), overthe 2 conditions (low and high attentional load) and 20 subjects.

A permutation test was used to identify the sites and time instants which showedsignificant differences between the high and low load conditions (Blair & Karniski,1993; Galán, Biscay, Rodriguez, Perez-Abalo, & Rodriguez, 1997). This distribution-free test does not require any assumptions about the correlation structure of thedata and provides exact p-values for any number of subjects. The procedure offeredempirical distributions which were used to obtain significance levels that control forexperiment-wise error, i.e. finding both the sites in which both conditions are signifi-cantly different (multivariate permutation test) and the time window in which thesedifferences were significant (univariate permutation test). A p = 0.05 significancelevel was adopted.

A lateralization index (LI) of �-band MSP was then calculated. This procedure,similar to that used by Thut et al. (2006) allows us to look at differential changesover the left vs. right hemisphere, incorporating the relative distribution of � activityover both hemispheres in one value. LI was calculated in each time point, conditionand subject according to the formula:

LI = MSP(Right) − MSP(Left)MSP(Right) + MSP(Left)

The index is negative when activity is more prominent over the left hemisphereand lower over the right (�-band MSP Right < �-band MSP Left) and positive whenthe opposite is the case (�-band MSP Left < �-band MSP Right). In order to assess ifthere were any differences between LI for different conditions the permute test wasused.

2.6. Correlational analysis between electrophysiological and behavioural LI

Correlational analyses comparing the behavioural and electrophysiologicalbiases were carried out. These compared the behavioural LI in the double simul-taneous stimulation with averaged windows of the LI of �-band MSP, for each ofthe attentional load conditions. The behavioural LI was calculated in essentially thesame way as the �-band MSP LI using the percentages of left first and right firstresponses. Four windows were created to average the LI of �-band MSP: from −200to 0 ms (baseline), from 1 to 280 ms (t1 to t2 interval), from 281 to 640 ms (post-t2first interval) and from 641 to 1000 ms (post-t2 second interval).

3. Results

3.1. Behaviour

3.1.1. t1 target discriminationAs intended over 95% discrimination accuracy was observed

across all subjects for every condition. In line with previous stud-ies, analyses of the t2 task were restricted to trials in which t1 wascorrectly identified in the high attentional load block.

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Fig. 2. The mean probability of ‘right-first’ responses as a function of SOA and atten-tional condition in the TOJ task. Negative SOAs indicate left-first presentation andzero SOA corresponds to simultaneous onset. Significant differences between atten-tional load conditions are mark with an asterisk. Error bars indicate±0.95 confidenceintervals.

3.1.2. t2 temporal order judgmentsAs expected in both low attentional load and high attentional

load conditions the probability of making ‘left-first’ or ‘right-first’responses increased as the SOA between the two stimuli increased.Additionally, when the targets were presented simultaneously inthe H condition participants were biased towards making a rightfirst response and in the L conditions responses were at the chancelevel (Fig. 2). A significantly increased proportion of ‘right-first’responses were made in the high load relative to low load con-dition when the left stimulus preceded the right by 120 ms (t = 2.1,p < 0.04) and 90 ms (t = 3.6, p < 0.01), suggesting that attention isbiased to the right in the high attentional load condition.

The percentage correct for each condition was submitted toa repeated measures analysis of variance (ANOVA) with ‘SOA’(excluding SOA = 0 ms), ‘Load’ (low attentional load vs. high atten-tional load) and ‘Side’ (‘right-first’ vs. ‘left-first’) as factors. Thisrevealed a main effect of SOA (F(1,19) = 6.9, p < 0.05) indicat-ing increased accuracy at longer SOAs. A main effect of Load(F(1,19) = 8.7, p < 0.01) indicating significantly reduced accuracy inthe high load (76%) relative to low load condition (85%) wasalso observed. Most importantly, a main effect of Side was seen(F(1,19) = 6.9, p < 0.05) with the percent of correct responses lowerfor the ‘left-first’ presentations (75%) than ‘right-first’ presentations(87%). In addition a significant Load by Side interaction (F(1,19) = 6.4,p < 0.05) was observed. Follow-up, analyses indicated significanteffect of Load for ‘left-first’ trials (F(1,19) = 9.7, p = 0.01) but not‘right-first’ trials, indicating that participants accuracy reductionsin the high load condition was limited to ‘left-first’ presentations.

To examine this further we transformed the data to allow usto compute variables used in previous studies of TOJ (Shore &Spence, 2005; Sinnett, Juncadella, Rafal, Azanon, & Soto-Faraco,2007; Zampini, Shore, & Spence, 2003). The percent correct for non-simultaneous trials was transformed to represent the percentageof ‘right-first’ responses. The raw scores of ‘right-first’ responsesas a function of SOA were transformed to their equivalent z-scoresusing a probit analysis, assuming a normal cumulative distribution(Finney, 1964). Transformed z-scores were obtained by applyingthe inverse of the standard normal distribution function to the

raw proportion scores. To include all trials in the inverse standardnormal distribution raw proportions of 1 and 0 were replaced by0.999 and 0.001, respectively. This transformation, allowed us toperform a linear regression with the transformed data across thefive SOAs. From the slope and intercept of the fitted line, two sum-mary statistics could be derived for each individual for both the lowand high attentional load conditions (Sinnett et al., 2007; Zampiniet al., 2003). These were:

i. The point of subjective simultaneity (PSS): the SOA between twostimuli at which observers report maximal uncertainty (mathe-matically equating to −intercept/slope).

ii. The just noticeable difference (JND): the SOA between twostimuli at which observers are able to correctly identify whichstimulus appeared first 75% of the time (mathematically equat-ing to 0.675/slope).

To compare conditions, the JND and PSS data were submitted tot-tests.

In the low attentional load condition a t-test revealed thatPSS values for the group did not differ significantly from zero(mean = −1.9 ms) suggesting that subjective simultaneity occurswhen the right and left circles appeared at the same time. How-ever, in the high attentional load condition the PSS values werestatistically different from 0 ms (mean = −48 ms, t = −3.5, p < 0.01),indicating that the circle on the left must be presented before thecircle on the right for both events to be perceived as simultane-ous. This indicates a rightward shift in attention for this condition.Indeed, a paired samples t-test (t = −5.4, p < 0.001) indicated a sig-nificant biasing of the PSS to the right in the high attentional loadcondition relative to the low attentional load condition. Moving onto the JND measure, a mean SOA of 34 ms between the 2 stimuli wasrequired for a correct discrimination order in the low attentionalload condition which rose to 74 ms in the high attentional load con-dition. As with the PSS measure JNDs differed significantly (t = 2.7,p < 0.05) between the low and high attentional load conditions (ABeffect).

3.2. Analysis of changes in the ˛-band spectral power

3.2.1. Trials with both t1 and t2Fig. 3 shows the time course of �-band MSP across electrodes.

Permutation tests revealed significant differences between �-bandMSP (p < 0.05) for high relative to low attentional loads for elec-trodes P3 (in the time window 185–715 ms) and T5 (in the timewindows 350–625 ms and 860–1000 ms), indicating that �-bandMSP was differentially modulated by attentional load at these sites.

A lateralization index was calculated by comparing two sym-metric posterior regions of interest (ROIs), comprising P3, T5 and O1and P4, T6, and O2 electrodes for the left and right hemisphere ROIs,respectively. As Fig. 3 illustrates, modulations in �-band MSP withattentional load were observed following t2 presentation, indexedby higher �-band MSP when t1 is ignored (low load) which wasreduced under high load conditions. The lateralization index (LI)(Fig. 3B middle panel) revealed a negative bias (increased activityin the left hemisphere) in the distribution of the �-band MSP in thelow load condition. In contrast, a positive bias was observed in thehigh load condition (increased activity in the right hemisphere).The permutation test revealed significant differences in LI betweenconditions which occurred in time interval from 455 to 480 ms.No hemispheric differences in absolute MSP values between highand low load conditions were observed prior to the onset of t1suggesting that these effects cannot be accounted for by baselinedifferences between the conditions.

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Fig. 3. (A) Time course of grand averaged �-band MSP as a function of attentional condition for all electrodes in t1 and t2 presentation trials. (B) �-Band MSP time courses asa function of attentional condition for the left ROI, the right ROI and the lateralization index are shown. The shaded area indicates significant differences (p < 0.05) betweenhigh and low attentional load conditions. The onsets of t1 (0 ms) and t2 (280 ms) are denoted on the time axis with vertical dashed lines.

3.3. Electrophysiological and behavioural correlation

Significant correlations between the �-band MSP andbehavioural LI scores were observed for the H condition forboth the post-t2 first interval (281–640 ms), r = 0.46, p = 0.04,d.f. = 19, and post-t2 second interval (641–1000 ms), r = 0.46,p = 0.04, d.f. = 19, time windows (see Fig. 4). These indicate thatsubjects who showed more positive �-band LI values tended tohave a more positive behavioural LI, suggesting a link between thedegree of perceptual bias to the right and increased alpha-bandactivity over the left hemisphere indicative of a relative inattentionto the left side.

3.3.1. Trials with only t1No hemispheric differences were observed in the time courses

of �-band MSP on trials in which the t2 target did not appear(Fig. 5). The general pattern of the LI time course for both thehigh and low load conditions (middle panel) showed an over-all leftward bias in the �-band MSP LI. A permutation testrevealed no significant differences in the �-band MSP LI betweenhigh and low load conditions. This provides additional evidencesuggesting that the rightward shift under high vs. low load isnot observed in the absence of lateralized stimulus processing,and thus may be generated by more reflexive attention mecha-nisms.

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Fig. 4. Correlations between the �-band MSP LI for the high attentional load condition and the behavioural LI in double simultaneous stimulation, in post-t2 first interval(281–640 ms) (left panel) and post-t2 second interval (641–1000 ms) (right panel).

4. Discussion

Our data convincingly show that increasing attentional load,here by the addition of the t1 target, led to a rightward biasingof temporal order judgement. Under conditions of low attentionalload the temporal order of the t2 stimuli were accurately perceived.However, the addition of the t1 task which recruited processingresources prior to the TOJ led to a marked impairment in judging therelative onset of the left and right targets, or impairment in detect-ing ‘arrival times’ (Sternberg & Knoll, 1973). One might anticipatethat reductions in attentional resources would lead to increaseduncertainty or ‘guessing’. If this were the case the number of leftfirst and right first responses should be approximately equivalentover a broader range of SOAs. Our behavioural data however, indi-cate that increasing attentional demands leads to a rightward shiftin the point of subjective simultaneity (PSS) such that left-sided tar-gets were perceived as appearing simultaneously with right-sidedobjects when they were in fact presented 48 ms prior to a righttarget. This suggests that reducing attentional resources does notsimply increase uncertainty, but rather leads to a specific rightwardshift in attention adding weight to the previous literature demon-strating specific rightward shifts in attention in both this (Pérez etal., 2008) and other paradigms (Bellgrove et al., 2004; Manly et al.,2005; Peers et al., 2006). In contrast to previous results (Pérez etal., 2008), we saw no convincing evidence of pseudoneglect underlow attentional load conditions. Our current experiment howeverwas not specifically designed to examine this issue and the reduc-tion of SOAs from five, used by Pérez and colleagues, to three maydiminish sensitivity to detect this phenomenon.

It appears that behavioural biasing of residual attention is asso-ciated with changes in the differential distribution of �-bandactivity between high and low attentional load conditions. Specif-ically we observed differences in the lateralization of �-band MSPunder conditions of low and high attentional load, with more �-band activity over the left hemisphere in the low load condition,which was reversed in the high load condition. Furthermore, acrosssubjects increased �-band activity over the right hemisphere wasassociated with a more pronounced rightward bias in behaviourin the high attentional load condition. This relationship betweengreater �-band MSP in the right hemisphere and more pronouncedrightward shifts in perceptual judgements suggests a link betweenthe perceptual bias to the right visual hemifield and relative inat-tention to the left.

Increased �-band spectral power has previously been observedin regions processing the unattended side of space (Kelly et al.,2006; Worden et al., 2000; Yamagishi et al., 2003). Furthermore, ithas been suggested that �-band synchronization serves to activelysuppress visual input from unattended locations (Rihs et al., 2007).Although we did not observe a significant leftward bias in atten-tion under low load attentional conditions (that might be predictedfrom the lateralized �-band pattern), previous results with this task(Pérez et al., 2008) and others (Bellgrove et al., 2004; Manly et al.,2005) report a mild leftward bias (pseudoneglect) in healthy pop-ulations under low attentional load. Our findings appear to suggestthat, even in the absence of a measurable behavioural asymme-try, asymmetries in �-band activity can be observed. This is in linewith an overall left bias in the distribution of attention related �-activity found by Thut et al. (2006) in healthy individuals. Our study

Fig. 5. Time courses of �-band MSP for t1-only trials as a function of attentional load condition for the left and right ROIs and the LI.

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A. Pérez et al. / Neuropsychologia 47 (2009) 41–49 47

suggests that symmetry of visual attention may be achieved withrelatively left lateralized �-band activity.

As attentional demands increase, changes in the distributionof alpha-band activity may result in either a decrement in theattention to left visual space or alternatively hyper-attention to theright. Our data and that of previous studies (Bellgrove et al., 2004;Manly et al., 2005) appear more consistent with the former expla-nation. They suggest that whilst symmetry in attention is associatedwith asymmetric �-band distribution (biased to left), asymmet-ric attention (rightward biasing) may be supported by shift in thedistribution of �-band activity to a more symmetrical pattern.

A natural product of biased-competition models of attention(Desimone & Duncan, 1995) is that the left and right hemispheresand thus the two sides of the visual field compete for attentionresources and therefore for the strength, priority and clarity of phe-nomenological representation. In line with this, inter-hemisphericcompetition in the broadly distributed network of frontal and pari-etal regions associated with spatial attention has been widelyreported (Hilgetag, Theoret, & Pascual-Leone, 2001; Rushworth,Ellison, & Walsh, 2001; Vuilleumier, Hester, Assal, & Regli, 1996).Our data, along with previous data reviewed in the introduction,suggests that reductions in attentional capacity lead to processingasymmetries. Using EEG we are able to show that this behaviouralasymmetry is associated with lateralized changes in alpha-bandactivity allowing us to observe a neural marker of inter-hemisphericcompetition.

When attention can be fully devoted to the stimuli (when thesubject is alert, not fatigued, and focussed on the task), the strengthsof the representations of target stimuli (competitive weights) ofcompeting stimuli in different parts of the visual field are approxi-mately equal resulting in a balanced awareness of targets on the leftand right. However, if attentional resources are depleted by drowsi-ness, fatigue, increased attentional demands or neural disruptions(Bellgrove et al., 2004; Manly et al., 2005; Peers et al., 2006) thenrightward bias is revealed.

Why then do reductions in attentional resources lead to a right-ward shift in bias? Our data showing a relative decrease in alphapower over the left hemisphere under high attentional load condi-tions is consistent with the idea that increases in attentional loadact to reduce inhibition of left hemisphere visual association cor-tex (Sauseng et al., 2005) under conditions of high load. It has beenargued that attentional biases result from suppression of competingstimuli (Worden et al., 2000) and that alpha activity is an indicatorof cortical inhibition (Hummel, Andres, Altenmuller, Dichgans, &Gerloff, 2002; Jensen, Gelfand, Kounios, & Lisman, 2002; Klimeschet al., 1998). Thus it is plausible that �-band desynchronizationunder high attentional load facilitates attentional gating of a com-peting stimulus from the right.

An alternative explanation suggests that hemispheric differ-ences in the expression of alpha based selection mechanisms (Kellyet al., 2006) could be a result of cognitive load affecting the right-lateralized arousal network (Paus et al., 1997). In line with this ithas been argued that pseudoneglect arises as a result of parietalasymmetries in the control of attention (Foxe, McCourt, & Javitt,2003). Under cognitive load resources are depleted resulting inreduction in arousal (Smit, Eling, & Coenen, 2004a; Smit, Eling, &Coenen, 2004b). Thus increases in task demands may act to reduceright hemisphere lateralized arousal processes (Peers et al., 2006),leading to general reduction in right hemisphere capacity and as aresult decreased ability for stimuli in the left hemisphere to com-pete for attentional resources. This explanation is also in line withthe increment of previously reduced �-band activity over the righthemisphere.

Previous EEG studies have demonstrated the involvement of �-band oscillations in the biasing of attention with spatial cueing

(Foxe et al., 2003; Kelly et al., 2006; Worden et al., 2000). Herewe extend those findings to show that �-band asymmetries canalso reflect a bias in the residual attentional deployment over spaceprovoked by high attentional load conditions. Although in spatialcueing attention is explicitly directed to one side of visual space andunder high perceptual load the spatial bias is implicitly induced,these two forms of attentional biases are likely to be sharing acommon neural mechanism. The time courses of effects with atten-tional cueing appear to imply that attentional control mechanismsare acting to bias attention. Our current data do not convincinglydemonstrate any measurable effect of attentional load prior to t2presentation, perhaps as a result of the relatively short (280 ms)duration between the two targets and the observation that alpha-band activity evolves slowly. However, the lack of a significantdifference between high and low load conditions in the absence ofthe t2 also appears to speak against a purely anticipatory of ‘controlbased’ explanation for our data, as such an explanation would pre-dict that when a second target is expected, the presentation of thefirst target alone should be sufficient to induce differences in antic-ipatory control mechanisms. Thus our data appear most consistentwith the notion of more stimulus driven attentional ‘expressionmechanism’ influencing bias.

A possible limitation of the present study is the fact that a similarelectrophysiological reactivity can be found in a somewhat higherfrequency band in the sensorimotor cortex during the prepara-tion of motor responses (Kaiser, Birbaumer, & Lutzenberger, 2001;Kaiser, Ulrich, & Lutzenberger, 2003), thus the rightward shift maymerely reflect some response difference between the two condi-tions. This is unlikely to explain our results, however, as responseswere balanced across both hands, avoiding either the consistentfindings relating right hemisphere activation/enhanced attentionto the left with use of the left hand (or vice versa) (Dobler etal., 2001; Failla, Sheppard, & Bradshaw, 2003). Additionally, ourfindings cannot be accounted for, or distorted by, the influence ofERP’s, because MSP is separable from phase locked EEG activity. It isassumed that MSP reflects induced oscillations that are modulatedby stimuli or events and which (in contrast to evoked rhythms) donot respond in a phase locked manner (Klimesch et al., 1998).

Here we obtain a rightward shift in attention under high atten-tional load conditions and lend further support for the involvementof alpha in the biasing of visuospatial attention. Our results con-tribute to mounting evidence that alpha oscillations are activelyinvolved in the biasing of visual attention (Foxe et al., 2003; Fu et al.,2001; Kelly et al., 2006; Thut et al., 2006; Worden et al., 2000). Welend further support to the idea that the depletion of attentionalresources induces a rightward shift in attention and suggest thatthis shift is operated by expression mechanisms in concordancewith a biased competition model.

Acknowledgements

The authors are grateful to Tonia Rihs and the two anony-mous reviewers for invaluable comments on earlier versions ofthis manuscript and to Agustín Lage for the advice concern-ing statistical analyses. This work was funded by MRC grantU.1055.01.001.00001.01.

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