RESEARCH ARTICLE

Paul M. Dockree Æ Mark A. Bellgrove

Fiadhnait M. O’Keeffe Æ Pauline Moloney Æ Lina Aimola

Simone Carton Æ Ian H. Robertson

Sustained attention in traumatic brain injury (tbi) and healthy controls:enhanced sensitivity with dual-task load

Received: 23 November 2004 / Accepted: 06 June 2005 / Published online: 26 July 2005� Springer-Verlag 2005

Abstract Poor sustained attention or alertness is a com-mon consequence of traumatic brain injury (TBI) andhas a considerable impact on the recovery and adjust-ment of TBI patients. Here, we describe the developmentof a sensitive laboratory task in healthy subjects(Experiment 1) and its enhanced sensitivity to sustainedattention errors in TBI patients (Experiment 2). The taskinvolves withholding a key press to an infrequent no-gotarget embedded within a predictable sequence of num-bers (primary goal) and detecting grey-coloured targetswithin the sequence (secondary goal). In Experiment 1,we report that neurologically healthy subjects are morelikely to experience a lapse of attention and neglect theprimary task goal, despite ceiling performance on thesecondary task. Further, attentional lapses on the taskcorrelated with everyday attentional failures and vari-ability of response time. In Experiment 2, the task dis-criminates between TBI patients and controls with alarge effect size. The dual-task yields more errors in bothgroups than a simple task involving only the primarygoal that is commonly used to detect sustained attentiondeficits in neurologically impaired groups. TBI patients’errors also correlated with everyday cognitive failuresand variability of response time. This was not the case inthe simple version of the task. We conclude that thedual-task demand associated with this task enhances its

sensitivity as a measure of sustained attention in TBIpatients and neurologically healthy controls that relatesto everyday slips of attention.

Keywords Dual-task Æ Sustained attention Æ Traumaticbrain injury Æ Prefrontal cortex

Introduction

Posner and colleagues (Posner and DiGirolamo 2000;Posner and Peterson 1990) have proposed that analerting or sustained attention system involving fronto-parietal regions of the right hemisphere of the brain isresponsible for modulating and maintaining the inten-sity of alert responding to incoming stimuli. This systemis essential for maintaining an intrinsic goal-directedfocus in otherwise unarousing contexts where exogenousstimuli are not present to increase alertness throughnovelty, demand or perceived difficulty (Robertson andGaravan 2004).

An established method of assessing this type of atten-tive responding, and one that activates the same rightfronto-parietal regions identified by Posner and Petersen,is the Sustained Attention to Response Task (SART)(Manly et al. 1999, 2002, 2003; Robertson et al. 1997). Inthis task, a predictable series of single digits (1–9) is pre-sented and subjects are required to press a response key toeach number except the number 3, which occurs predict-ably at every ninth digit. A Positron Emission Tomogra-phy (PET) study (Manly et al. 2003) showed that this taskincreased activation in both the right dorsolateral pre-frontal cortex and the right superior/posterior parietalcortex compared to a more challenging version of theSART in which the numbers are presented randomly.Since the unpredictable nature of the random sequence islikely to exert an alerting effect, the heightened activitywithin fronto-parietal networks in the fixed, versus ran-dom, version of the SART supports a view that the pre-frontal cortex acts to maintain endogenous alertness

P. M. Dockree (&) Æ M. A. Bellgrove Æ F. M. O‘KeeffeP. Moloney Æ L. Aimola Æ I. H. RobertsonDepartment of Psychology Trinity CollegeInstitute of Neuroscience, Trinity College Dublin,Dublin, 2 IrelandE-mail: dockreep@tcd.ieTel.: +353-1-6083083Fax: +353-1-6712006

M. A. BellgroveDepartment of Psychiatry, Trinity College Dublin,Dublin, 2 Ireland

S. CartonNational Rehabilitation Hospital, Rochestown Avenue,Dun Laoghaire, Co. Dublin, Ireland

Exp Brain Res (2006) 168: 218–229DOI 10.1007/s00221-005-0079-x

under monotonous task demand but is less-required un-der more alerting or challenging task demands.

The SARTfixed is exceptionally sensitive to frontal lobedamage associated with traumatic brain injury (TBI)suggesting that disruption of right hemisphere attentionsystems is a distinct possibility in the context of the diffusedamage that characterizes TBI. Poor performance on theSARTfixed in brain-injured patients may be associatedwith impaired right-prefrontalmodulation of sub-corticalnoradrenergic structures. Recent PET studies (Sturmet al. 1999, 2004) suggest that an extended right hemi-sphere network is involved in sustained attention includ-ing the right anterior cingulate, the right dorsolateralprefrontal cortex, the right inferior parietal lobule withprojections to the thalamus and noradrenergic brainstemtargets. Sturm et al. propose that the right hemispherebrain structures exercise top-down control, via the thal-amus, on noradrenergic structures in the brainstem.

Increases in attentional performance are associatedwith increased thalamic activity under conditions of lowarousal (Portas et al. 1998) suggesting that enhancedtop-down control is required to perform a task underconditions of low arousal. Thalamo-cortical circuits alsomodulate the expression of oscillations in the alpha band(8 – 13 Hz). An increase in metabolic activity in thethalamus is associated with a reduction in alpha power(or desynchronization) that is indicative of enhancedcognitive performance (Lindgren et al. 1999; Lopes daSilva et al. 1980). Recent evidence (Dockree et al. 2004)suggest that TBI patients (with moderate to extremelysevere post-traumatic amnesia, PTA) fail to show alphadesynchronization at strategically opportune pointsduring the SARTfixed suggesting that damage to eithercortico-cortical or thalamo-cortical networks after braininjury disrupts the ability to enhance the intensity ofalert responding during the SARTfixed.

The consequences of failures of the sustained atten-tion system in everyday life can be dramatic. Forexample, signals passed at danger on the railways haveresulted in serious accidents that have largely beenattributable to human error. It is therefore important tounderstand how individual differences in the capacity forsustained attention might relate to everyday slips ofattention. We have previously noted a relationship be-tween commission errors on the random version of theSART and self-reported everyday attentional problems,as measured by the Cognitive Failures Questionnaire(CFQ) (Robertson et al. 1997). We have hypothesized,however, that the SARTfixed may be a more appropriateexperimental analogue for everyday slips of attention,since in this task particularly, one must maintain alert-ness in the context of routine action. Nevertheless, ourexperience of the SARTfixed suggests that performance isnear floor for many healthy adults (Dockree et al. 2004;Manly et al. 2003).

In the present study, in order to better characterizethe relationship between sustained attention and every-day absentmindedness, we developed a dual-task versionof the SARTfixed by embedding a continuous perfor-

mance task (CPT) within the SARTfixed,hereafter calledthe Dual-task Attention to Response Task (DART). Wereasoned that, since CPTs are thought to challenge thesame fronto-parietal attentional networks (Sturm et al.2004) that provide a dual-task requirement wouldmaximally challenge this system and reveal individualdifferences in the capacity for sustained attention. Thegrey detection task represents a simple CPT and low-demand CPTs were shown to activate the same fronto-parietal network as the SARTfixed. We propose that thesustained attention system will be challenged in anadditive fashion by these two similar tasks.

Stuss et al. 1995) have argued that the reducedexogenous stimulation that characterizes sustainedattention tasks (i.e., simply monitoring for a infrequentstimulus) can make individuals vulnerable to alternativecompetitors for processing resources. That is, processingresources may be allocated to distractible trains ofthought or irrelevant environmental distractors, whichwill vary with the individual and the environment andwill be uncontrolled factors during the task. We proposethat the DART will increase the sensitivity of the basicSART by including ‘‘built-in’’ distractors (grey num-bers) that will serve to keep subjects on-task and preventcapture by uncontrolled factors allowing sustainedattention to the primary task goal to be measured withgreater sensitivity. For a similar approach, see Manlyet al. (2001) rationale for the development of the Score!and the Score DT, both sub-tests of the Test of EverydayAttention for Children (TEA-ch).

Although, we conceived the sustained attention sys-tem as a functionally, independent right-lateralizednetwork responsible for regulating the intensity ofalertness, it is important to stress that this system worksin the service of current task goals thus close interactionsbetween goal representations and the vigilant state is tobe expected. For instance, in the context of the SART,successfully withholding to the ‘3’ becomes especiallyreliant on alertness if the task goal has been allowed todecay. Under these conditions the engagement of thesustained attention system is necessary to support reac-tivation of the task goal. Consequently, we argue thatsustained attention is an interactive system that cannotbe examined in complete isolation from other aspects ofcognitive control including selective attention, goalactivation and task switching. For further discussion ofthe relationship between alertness and other executivesystems, see Robertson and Garavan (2004).

The impact of TBI on everyday attentional problemsis well-documented (McKinlay 1981; Richardson 2000)and in the present study we also sought to replicate andextend our characterization of alert responding in TBIpatients by examining their performance on the dual-task version of the SARTfixed. We hypothesized that theadditional demands of this modified task will showgreater sensitivity to deficits of sustained attention.

Experiment 1: Development of a task sensitive to everydayaction slips In this study, the dual-task load of the

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DART was increased parametrically across three con-ditions (7, 14, 21 grey digits, respectively). The rationalefor this is as follows: the standard SARTfixed involves alow level of exogenous activation for the goal-relevanttask-set (i.e., updating the number sequence and select-ing the ‘3’) and this makes it vulnerable to off-task di-stractors, both environmental and cognitive. Toreiterate, the DART measure was designed to increasethe sensitivity of the basic SARTfixed by including ‘built-in’ distractors in the form of grey digits. Consequently,we instructed subjects to constrain monitoring demandsto two simple goals and further, we requested subjects toprioritise grey detection in order to compete for avail-able processing resources available for selecting andwithholding to the ‘3’. It is predicted that the demand onprocessing resources will increase across conditions. Inaddition, a task of increased attentional load shouldincrease the relationship between task performance andeveryday cognitive failures as measured by the CFQ.

Method

Participants

Sixteen (five male) neurologically normal, paid volun-teers, aged 19–23 participated. All subjects gave writteninformed consent, and the Psychology DepartmentEthics committee at Trinity College Dublin approved ofthe procedures. All subjects reported normal or normal-to-corrected vision and right-handedness.

Materials

Sustained attention tasks The participants undertooktwo tasks of sustained attention: the SARTfixed and the

DART which is a dual task variant of the SARTfixed. Inthe SARTfixed, digits were presented sequentially from 1through 9 (see Manly et al. 2003). For each block, 225digits were presented sequentially (repetitions of the 1–9sequence) over a 6.3-min-period. Each trial beganwith thepresentation of a digit for 494 ms followed by a 125 msmask consisting of a ring with a diagonal cross in themiddle. Next, a response cue was presented for 63 mscomposed of a ring with an emboldened diagonal cross.Finally, a second mask was presented (identical to thefirst) for 494 ms1. Figure 1 displays the trial sequence. Theparticipant was instructed to respond with a left mousepress as close to the response cue as possible followingeach digit (go-trials) with the exception of the 25 occasionswhen the digit 3 (target) appeared. The response cueserved to reduce the influence of inter-individual differ-ences in RTs. That is, excessively fast individuals maymake speed-related errors, whereas excessively slowindividuals will not be disadvantaged in this way. Theresponse cue served to normalize the distribution of RTsacross the group but was not intended to influence intra-individual variability in RT. Previous research demon-strates that response-locking does not alter intra-indi-vidual RT patterns that are informative to the likelihoodof error (Bellgrove et al. 2004; Dockree et al. 2004).

An inter-trial-interval (ITI) of 494 ms followed eachtrial and consequently the period from digit onset todigit onset was 1,670 ms2. In keeping with Robertsonet al. (1997), five randomly allocated digit sizes were

Fig. 1 Sequence of events for each trial

1Presentation timing was determined by screen refresh rates. Thevalues presented were converted from screen refresh rates (or ticks)to the milliseconds.2The longer trial presentation time compared to earlier versions ofthe SART was used to accommodate the mask and response cue.

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presented to increase the demands for processing thenumerical value and to minimize the possibility thatsubjects would set a search template for an unspecifiedperceptual feature of the no-go trial (‘3’). Digit sizeswere 8 mm, 11 mm, 14 mm, 17 mm and 20 mm,respectively. The diameter of mask-1, response cue andmask-2 were each 23 mm. The digits, masks and re-sponse cue were presented centrally in white on a com-puter monitor against a black background. The screen(320 mm · 240 mm: Dell PC) was positioned approxi-mately 40 cm from the participant. The experimentgenerator used was DMDX3. The SART was precededby a practice trial including 27 trials with three criticalno-go targets.

In the DART, a secondary CPT was embeddedwithin the basic design of the SARTfixed.In addition topressing the left mouse button to go-trials and with-holding a response to no-go targets (‘3s’), participantswere also required to make a right button press upondetection of grey-coloured digits. In order to challengeavailable processing resources during the task but not tochallenge performance in the period before and imme-diately after the presentation of a target (during thepresentation of 1 through 4) the presentation of grey-coloured digits was restricted to numbers 5 through 9.

Grey digits were created in Microsoft Paint with aluminance of 120 and a hue of 160. Three versions of theDART were created, each differing in the frequency ofoccurrence of the grey digit and thus parametricallymanipulating the continuous performance dual-taskload:

1. 193 go-trials, 25 targets and 7 greys (total = 225)2. 186 go-trials, 25 targets and 14 greys (total = 225)3. 179 go-trials, 25 targets and 21 greys (total = 225)

All other aspects of the test, namely the trial dura-tion, ITI, stimulus size and software specificationswere identical to the SARTfixed.

The DART was preceded by a practice block thatincluded 27 go-trials, 3 targets and 6 greys. Participantshad to achieve 100% accuracy on the practice blockbefore they could proceed to test. Therefore, if neces-sary, the practice block was repeated until participantperformance was at the 100% criterion level.Cognitive failures questionnaire The CFQ comprises 25questions whereby the participants rate the frequency(on a 5 point Likert scale) with which they make cog-nitive errors in everyday scenarios. For example, ‘‘doyou start doing one thing at home and get distracted intodoing something else (unintentionally)?’’ (Broadbent,Cooper, Fitzgerald and Parkes, 1982).

Design/procedure Participants initially completed theCFQ questionnaire. Subsequently, the practice block forthe SARTfixed was administered followed by a singleblock of SARTfixed. Participants received the followinginstructions for the SARTfixed:

‘In this task you will see a series of numbers presentedin sequence from 1 to 9. After each number is pre-sented, you will see a cross in the centre of the screen.The cross will appear to flicker. Please press the leftmouse button after each number when you see thecross flicker. Please do not respond following thenumber 3.’

After completion of the practice and test for theSARTfixed, participants began the practice block for theDART. As described above, 100% accuracy was re-quired before the participants could proceed to test; thepractice block was repeated if this criterion level was notmet. Participants were given the following instructionsfor the DART:

‘In addition to withholding your left mouse responsefollowing the number 3, I’d like you to press the rightmouse button whenever you see a grey-colourednumber. Please be especially careful not to miss thegrey-coloured numbers’

All participants were trained to adopt the correctprocedure of pressing the left mouse button to Go-trials,the right mouse buttons to grey trials and withholding tothe number 3. After practice, participants completedthree versions of the DART. These three versions dif-fered in terms of the number of grey numbers presentedwith 7, 14 and 21 grey items, respectively. Hereafter,these conditions are referred to as DART+7,DART+14 and DART+21. Counterbalancing ensuredthat each DART condition occurred first, second andthird equally often. The SART was always completedfirst to avoid the possibility that participants would notmistakenly monitor for grey items if they had previouslyundertaken a DART block.

Results

Validating the DART

Commission errors are defined as false key responses onthe ‘3’. Table 1 shows the mean number of commissionerrors as a function of task. A one-way repeated mea-sures ANOVA was conducted with Task (SART,DART+7, DART+14, DART+21) as the within-subjects factor and errors of commission as the depen-dent variable. A main effect of Task was apparent, F(3,45)=5.15, P=0.004. Within-subjects contrasts demon-strated that errors of commission were significantlygreater for DART+7 (P=0.006) and DART+21(P=0.01) compared to the SART. The differences be-tween DART+14 and SART were just short of signifi-cance but in the expected direction (P=0.057). Inter-correlations between each version of the DART and theSART, with respect to commission errors, demonstratedsignificant relationships between all tasks with the3DMDX display software, The University of Arizona.

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exception of SART and DART+14 that falls short ofsignificance (see Table 2). These relationships suggest allversions of the DART and the SART tap similarunderlying attentional processes.

The data confirm that the practice block was suc-cessful in achieving a high accuracy for grey perfor-mance, irrespective of condition. The mean number ofcorrect detections to grey items approached ceiling ineach task: DART+7 (6.88 SD=0.50), DART+14(13.69 SD=0.60) and DART+21 (20.75 SD=0.58).

Self-reported cognitive failures and errors of commission

Subjects’ mean CFQ-reports were 49.81 (SD=10.19,range=44). We examined the relationship between CFQscores and SART performance. Commission errors onDART+21 and CFQ scores were positively correlated(r=0.528, P=0.035). Increased errors of commission onDART+21 are therefore related to a higher number ofreported cognitive failures in everyday life. The CFQ didnot correlate with the other two versions of the DART(P>0.05).

Intra-individual variability

Increased variability of response time in TBI patientshas been shown to be associated with impaired atten-

tional control (Stuss et al. 1999) Further work of Stusset al. (2003) suggested that focal brain damage affectingthe dorsolateral prefrontal cortex underlies increasedintra-individual variability. These findings suggest thatdorsolateral prefrontal activation seen during the SART(Manly et al. 2003) may modulate variability of alertresponding and this function may be disrupted by braininjury. Intra-individual variability many therefore be animportant marker for sustained attention and it isexamined here.

To obtain a measure of variability, participants’standard deviations are divided by their mean go-trialresponse time giving a coefficient of variation (CofV) inorder to normalize for the effects of the absolute mag-nitude of their RTs. Significant relationships betweenCofV and commission errors were found across all threeversions of the DART. In the SARTfixed, however, CofVdid not correlate with commission errors. Mean CofVand correlations between CofV and commission errorsfor each task are reported in Table 1.Experiment 2: Does the DART discriminate TBIs fromneurologically normal controls? It is predicted that theadditional demands of the DART will show greatersensitivity to deficits of sustained attention. We haveshown in Experiment 1 that The SART and DART+21are highly correlated suggesting that they tap a similarunderlying system. In the current experiment, we inves-tigate lapses of attention in TBI patients’ and controlsand examine the influence of intra-individual variabilityas a possible contributing factors to these errors.

Method

Participants

Twenty nine TBI participants and 32 non-brain-injuredcontrol participantswere recruited for this study. TheTBIpatients were recruited from the National RehabilitationHospital, Dun Laoghaire, coDublin. Clinical data for theTBI patients are presented in Table 3 and included thefollowing: Cause of brain injury, PTA severity, Glasgowcoma scale (GCS) severity, number ofmonths since injuryand location of brain damage. To summarize, the cause ofinjury fell into 4 categories (Road traffic accident, workaccident, assault or fall). Two TBI patients had ‘mild’(<1 h), 2 had ‘severe’ (1–7 days) PTA, 13 were classed as‘very severe’ (7–28 days) and 11were classed as ‘extremelysevere’ (>28 days). PTAwas unavailable for one patient.Records from the GCS were available for 22 of the pa-tients. Two patients were registered as ‘mild’, six patientswere ‘moderate’ and 14patientswere ‘severe’. The averagenumber ofmonths since injury was 34.81 (SD±21.94). Ofthe 29 patients, 17 of the patients’ hospital records re-ported direct frontal lobe damage as part of their injury(eight right frontal, four left frontal, three bilateral andtwo unspecified). Patients also exhibited damage in pari-etal, temporal and occipital areas and sub-cortical dam-age to the basal ganglia and the cerebellum (see Table 3).

Table 1 Mean commission errors and mean CofV as a function oftask and correlations between commission errors and CofV foreach task

SART DART+7 DART+14 DART+21

Mean commission errorsMean 1.63 3.13 2.75 4.00SD 1.89 2.36 2.27 3.92Range 6.0 8.0 8.0 17.0Mean coefficient of variation (CofV)Mean 0.131 0.143 0.145 0.147SD 0.031 0.052 0.044 0.048Range 0.11 0.18 0.14 0.14Correlations: CofV CofV CofV CofVCommission errors r=0.19 r=0.64 r=0.72 r=0.54

P=0.475 P=0.007** P=0.002** P=0.032*

** P<0.01; * P<0.05

Table 2 Pearson correlations between the SART, DART+7,DART+14 & DART+21

SART DART+7 DART+14 DART+21

DART+7 r=0.637P=0.008**

DART+14 r=0.459 r=0.816**P=0.074 P=0.0001**

DART+21 r=0.576 r=0.684 r=0.744P=0.020* P=0.003** P=0.001**

** P<0.01; * P<0.05

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The groups were matched according to gender, ageand years in education. Characteristics of both the TBIgroup and the control group are outlined in Table 4.The TBI patients had not experienced a major psychi-atric disorder, a drug or alcohol dependency, a pre-trauma history of epilepsy or any other neurologicaldisorder. The control participants also fulfilled the latterrequirements and additionally, had never suffered loss ofconsciousness from a head injury. Participation in thestudy was approved by the ethics committee of theDepartment of Psychology, Trinity College Dublin andby the National Rehabilitation Hospital, Dun Laogh-aire, co Dublin. All participants signed an informedconsent form before the beginning of the experiment.

Materials

To assess cognitive and emotional functioning thatpertain to everyday events the Hospital AnxietyDepression (HAD) scale and the CFQ (see Experiment1) were administered to all participants. The HAD(Zigmond and Snaith 1983) scale comprises 14 items,

seven of which reflect anxiety levels and seven corre-spond to depression levels.

A version of the DART was presented to TBI pa-tients and control subjects. 225 single digits from one tonine were centrally presented. Each digit was presented25 times and was displayed for 580 ms followed by aninter-stimulus-interval (ISI) of 920 ms. Digits were pre-

Table 3 Clinical data for TBI patients

TBI Patient TBI cause TBI severity(PTA)

TBI severity(GCS)

Monthssince TBI

Location of damage

AC RTA- Car Extremely severe Severe 32 Frontal cyst, otherwise normal CTAMB Fall Extremely severe Moderate 31 Right Subdural haemotoma,

Right frontalBE Assault Very severe Severe

11 Left temporal region,cerebellar haemorrhage

BF Fall Extremely severe Severe 13 SAH, Right temporal, Left parietalCL RTA- Car Extremely severe Moderate 67 SAH, Right occipital, Right HemisphereCMG RTA- Motorbike Extremely severe Severe 38 Left FrontoparietalCOD RTA- Car Extremely severe N/A 97 Bilateral frontal, Left occipitalDD RTA- Car Very severe Moderate 34 Normal CT scanDF RTA- Car Extremely severe N/A N/A N/ADP RTA- Motorbike Very severe Severe 9 Right frontal lobe, Normal CTER1 Fall Very severe Severe 21 Right Frontal, SAHER2 RTA-Bicycle Very severe Mild 28 Right Temporal ContusionsER3 RTA- Car Very severe Severe 58 Bilateral Frontal, SAH, DAIFL RTA- Car Extremely severe Severe 38 SAH, left frontal, left superior temporal,

left occipitalGB RTA- Car Mild N/A 84 DAIGC Fall Very severe Severe 44 Right frontal ICHGH RTA- Car Very severe Severe 28 Frontal Lobe, SAH, parietal, occipitalGL Fall Severe N/A 39 Right FrontalGM RTA- Car Very severe N/A 28 Right fronto-parietal, DAIJC RTA- Motorbike Very severe Moderate 25 Left fronto-temporal haemotomaJC2 RTA- Car Extremely severe Moderate 34 Normal CT, DAIJG N/A Severe N/A N/A N/AJG2 RTA- Motorbike Extremely severe Severe 29 SAH, bilateral temporal,JK Work Accident Mild N/A N/A N/AKM Assault Very severe Moderate 13 Right fronto-parietalMOM Assault Very severe Mild 19 N/AOW RTA- Motorbike N/A Severe 23 Frontal Bilaterally, Basal Ganglia,

temporal RightPJD Assault Very severe Severe 53 Left frontal, left subdural haemorrhageRB RTA- Car Extremely severe Severe 9 Right Frontal, Left occipital, DAI

Table 4 Participant characteristics

TBIs (n=29) Controls (n=32)

Participant characteristicsGenderM 26 24F 3 8Age (years)Mean 28.66 29.69SD (8.81) (12.35)Range (31.0) (45.0)Level of educationPrimary 5 6Secondary 10 13Tertiary 14 13

PTA Post traumatic amnesia (Mild: <1 hour; Moderate: 1–24 hours; Severe: 1–7 days; Very severe: 7–28 days; Extremely se-vere: >28 days), GCS Glasgow coma scale (Mild: >13; Moderate:

9–12; Severe: <8), RTA Road traffic accident, DAI Diffuse axonalinjury, SAH Subarachnoid haemorrhage, ICH Intracerebralhaemorrhage, N/A Not available

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sented 0.25� above a central white fixation cross on ablack background. The task specifications were pro-grammed and stimuli were delivered using DMDX.These modifications served to reduce the perceptual loadfor TBI patients by removing the response cue demandsand increase the trial duration to account for slowerinformation processing in the TBI group. All stimuluscharacteristics including colour and size were identical toExperiment 1.

Design/procedure

Subjects initially completed the CFQ and the HAD. Allsubjects subsequently undertook one block of theSARTfixed and DART+21. The presentation of theseblocks was counterbalanced across participants. Inaccordance with Experiment 1, a practice session, inwhich 100% response accuracy was required, precededthe test blocks. Participants received the followinginstructions for the SARTfixed:

‘In this task you will see a series of numbers presentedin sequence from 1 to 9 above a central fixation cross.Please press the left mouse button in response to eachnumber Please do not respond following the number3.’

Participants were given the following additionalinstructions for the DART:

‘In addition to withholding the left mouse responsefollowing the number 3, I’d like you to press the rightmouse button whenever you see a grey-colourednumber. Please be especially careful not to miss thegrey-coloured numbers’

Results

Group differences

TBI patients reported a greater frequency of everydaycognitive failures as measured by the CFQ-for-self,compared to control subjects, t(59)=3.12, P=0.003.There was no significant between-groups effect for theCFQ-for-other, t(54)=1.58, P=0.1204. Emotionalfunctioning in TBI patients, as measured by the HAD,revealed higher levels of anxiety, t(59)=3.0, P=0.004,and depression, t(59)=5.88, P=0.0001, compared tocontrols. Mean scores and standard deviation are pre-sented in Table 5.

Table 5 also reports the mean number of commissionfor TBI patients and controls. A mixed repeated mea-sures ANOVA with group (TBI, control) as the betweensubjects factor and task (SART, DART) as the within-subjects factor. A main effect of group demonstrated

that TBI patients made significantly more commissionerrors compared to controls, F(1,58)=9.58, P=0.003.Further, a main effect of task showed that the DARTproduced significantly more errors than the SART,F(1,58)=30.46, P=0.0001. There was no Group · Taskinteraction, F(1,58)=2.61, P=0.111. For each group,effect sizes for Task were calculated seperately. For thecontrol group, Cohen’s d = 0.925 and for the TBI pa-tients, Cohen’s d = 0.896 indicating that large effectsizes were apparent discriminating DART and SARTperformance in each group.

Commission errors, cognitive failures and emotionalfunctioning

Correlations between commission errors on the SARTand DART and self-reported cognitive failures wereexamined. There was no relationship between CFQ-selfand commission errors for the SART in the controlgroup (r = �0.139, P=0.449) or the TBI patient group(r=0.108, P=0.586). There was also no relationship

Table 5 Mean questionnaire scores, mean commission errors andmean CofV as a function of group (TBIs, controls)

TBIs Controls p value

QuestionnairesHospital anxiety depression scale (HAD)HAD anxietyMean 9.48 6.22 0.004**SD 5.01 3.41Range 18 11HAD depressionMean 7.69 2.38 0.0001**SD 4.73 1.86Range 18 7Cognitive failures questionnaire (CFQ)CFQ-selfMean 47.97 32.06 0.003*SD 25.25 11.26Range 89 55CFQ-otherMean 14.33 10.38 0.120SD 8.64 9.97Range 29 54Sustained attention tasksSARTfixed

Commission errorsMean 2.14 1.19 0.041*SD 2.05 1.33Range 7 5Coefficient of variationMean 0.267 0.220 0.043*SD 0.084 0.082Range 0.43 0.41DARTCommission errorsMean 5.00 2.75 0.009**SD 4.02 1.98Range 17 8Coefficient of variationMean 0.246 0.190 0.003**SD 0.082 0.056Range 0.30 0.25

4CFQ-for-other scores were unavailable for three control partici-pants and two TBI patients.

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between CFQ-self and DART commission errors for thecontrol group (r = �0.103, P=0.574). However, a sig-nificant positive correlation between DART commissionerrors and CFQ-self reports was apparent in the TBIgroup (r=0.385, P=0.039).

To ensure that our group differences for commissionerrors were not the result of higher levels of reportedanxiety and depression in the TBI patients, we correlatedHAD-anxiety and HAD-depression with commissionerrors for the SART and DART in each group. For theSART, commission did not significantly correlate withHAD-anxiety (Controls: r = �0.087, P=0.635; TBIs:r=0.078, P=0.693) or HAD-depression (Controls:r=0.263, P=0.145; TBIs: r = �0.173, P=0.378) foreither group. For the DART, there was not relationshipbetween errors and HAD-anxiety for controls but a non-significant trend was apparent in the TBI group (Con-trols: r = �0.101, P=0.581; TBIs: r=0.348, P=0.065).Commission errors and HAD-depression did not cor-relate for either group (Controls: r = �0.175, P=0.339;TBIs: r=0.115, P=0.554).

Mean response times

Response times were analysed separately for the SARTand the DART and are presented in Fig. 2. For theSART, a 2-way mixed factorial ANOVA with Group(TBIs, controls) as the between-subjects factor and Re-sponse-type (go-trial RT, commission error RT) as thewithin-subjects factor was conducted. A significant maineffect of Response-type, F(1, 37)=9.24, P=0.004, wasdriven by longer commission error RTs compared to go-trial RTs. A main effect of group was short of signifi-cant, F(1,37)=3.43, P=0.072, with a trend towardsfaster RTs for TBI patients compared to controls. NoGroup · Response-type interaction was observed, F<1.For DART RTs, a second Group · Response-typeANOVA was conducted. Response-type included theadditional level of grey-trial RT. No main effect ofGroup, F(1,53)=1.24, p=0.271, or Group · Response-type interaction, F(2,106)=1.69, p=0.190, was appar-ent. Response-type showed a significant main-effect,

F(2,106)=139.38, P=0.0001. Simple contrasts showedthat mean grey-trial RT was significantly longer thancommission error RT or go-trial RT irrespective ofgroup (both P<0.0001). Mean commission error RTand go-trial RT did not significantly differ from eachother (P=0.947).

Intra-individual variability by group

In Experiment 1, high response variability (as measuredby the CofV) was shown to be associated with an in-creased number of commission errors. In the currentexperiment, we examined whether the CofV differedbetween TBI patients and controls. Independent samplest-tests confirmed that TBI patients exhibited signifi-cantly higher mean variability in their Go-RTs duringthe SART, t(54)=2.07, P=0.043, and the DART,t(59)=3.12, P=0.003. Furthermore, pair-samples t-testsrevealed that mean variability was higher during theSART than the DART for both TBI patients,t(23)=2.24, P=0.035, and controls, t(31)=2.06,P=0.048. Mean scores and standard deviation are pre-sented in Table 5.

The relationship between response variability andcommission errors was examined for the SART andDART for each group. There was no significant rela-tionship between response variability and commissionerrors during the SART for either the control group(r=322, P=0.072) or the TBI group (r = �0.038,P=0.862). During the DART, the control also failed toshow a relationship between response variability andcommission errors (r=0.072, P=0.693). However, inthe TBI patients’ group, response variability increasedlinearly with number of commission errors (r=0.500,P=0.006). Figure 3 depicts this relationship.

Discussion

The findings from Experiment 1 demonstrate that slipsof attention during a dual-task paradigm that requiresalert responding during routine action increased the

Fig. 2 Mean response times(RTs) during the SARTfixed andDART tasks as a function ofgroup

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number of errors for neurologically healthy adults.Further, the task that exerted the highest dual-task load(DART+21) and yielded the highest number of errorsalso correlated with everyday reported errors measuredby the CFQ. This relationship suggesting that theDART is a useful experimental analogue for real-lifeslips of attention that captures variability within thenormal range of behaviour. An analysis of the responsetime data also revealed significant relationships betweengo-trial RT variability and commission errors across allthree versions of the DART. In each case, high RTvariability was associated with increased errors ofcommission in healthy adults and, as has been arguedelsewhere, (Bellgrove et al. 2004; Stuss et al. 1999) intra-individual response variability may provide a useful in-dex of the efficiency of attentional control.

In Experiment 1, the DART appears to be moresensitive to individual differences in sustained attentionin neurologically normal adults than the originalSARTfixed. We argue that additional monitoring for greyitems represents a secondary task-set which drawsattention away from the primary task-set of withholdinga response to the ‘3’ leading to more errors of commis-sion. The presentation of grey digits was always re-stricted to numbers 5 – 9, thus the upcoming period tothe target-trial (1, 2...) was free from the secondary taskdemand giving subjects the opportunity to switch theirtask-set back to the primary task of withholding theirresponse on the ‘3’. An inability to disengage from thesecondary task-set and to deploy attention to the pri-mary task during the upcoming period may, in part, beresponsible for increased commission errors. The factthat the DART+21 correlated with reported everydaycognitive failures suggests that it might be analogous to

real life dual-task situations such as failure to hearpeople speaking to you when you are otherwise engagedor getting distracted by a new activity and neglecting tofinish what you are currently doing. Under these cir-cumstances, maintaining a sufficient level of alertnesswould enable one to remain sensitive to incominginformation and deploy attention appropriately. Inter-subject differences in everyday absentmindedness maycome to be seen as underscored by individual differencesin the efficiency with which fronto-parietal areas exerttop-down control. Such a hypothesis is amenable totesting with functional imaging.

In Experiment 2, we extended our analysis of alertresponding in TBI patients and matched controls byexamining their performance on the SART and theDART. The key findings showed that patients exhibitedsignificantly more errors of commission in both taskscompared to healthy controls and, irrespective of par-ticipant group, the DART yielded significantly morecommission errors than the SART. A large effect sizediscriminating SART and DART performance wasapparent in both TBI and control subjects (Cohen’sd>8). In line with previous studies (Manly et al. 2003,1999; Robertson et al. 1997) we argue that the higherprevalence of commission in TBI patients is associatedwith transient ‘drifts’ of controlled processing leading toa more automated mode of responding. Frontal, pre-frontal and cingulate hypoperfusion and damage tosubcortical structures were linked with diffuse axonaldamage in TBI patients (Bonne et al. 2003; Fontaineet al. 1999) suggesting that the neural substrate of theSARTfixed may have been disrupted, along with otherareas, as a result of brain injury. Consequently, theright prefrontal cortex of TBI patients may be less

Fig. 3 Scatter plot depicting therelationship between DARTcommission errors and DARTresponse variability in TBIpatients and controls.

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efficient at controlling the maintenance and intensity ofalertness.

Evidence from Experiment 2 also supported the claimthat the DART may serve as a useful experimentalanalogue for everyday attentional slips. We found asignificant positive correlation between DART com-mission errors and the CFQ in the TBI patients. Bycontrast, the SART did not show this relationship withreported cognitive failures. Unexpectedly, however, theDART-CFQ correlation was absent in the healthycontrols in Experiment 2 despite this relationship beingpresent in Experiment 1. This discrepancy can be ex-plained, in part by the fact that the healthy subjects inExperiment 2 reported fewer cognitive failures andexhibited a fewer number and smaller range of errors onthe DART compared to those in Experiment 1. Thus, alower frequency of everyday attentional problems to-gether with superior DART performance may explainthe absence of the DART-CFQ relationship in healthycontrols in Experiment 2. It is possible that the longertrial duration, intended to benefit patients’ slowerinformation processing on the DART, may have facili-tated healthy control’s performance in Experiment 2.

The comparable ceiling performance for grey targetdetection in TBI patients and controls suggests that bothgroups met the embedded secondary task demandeffectively. The response time analysis revealed a similarpattern of responses for all subjects with longer RTs togrey targets than go-trials. This RT switch-cost was ofsimilar magnitude in TBI and control subjects. Giventhat grey detection and the RT strategy were identical inpatients and controls, why does the additional load ofthe DART confer disproportionate error rates on trial 3?The DART requires coordination between differentmonitoring task-sets (go-response, no/go response andgrey-response) that are executed on separate trials.Commission errors on the ‘3’ will arise if subjects fail toactivate the primary task-set or if they fail to disengagemonitoring for grey items and neglect the primary task.

We argue that TBI patients may be less able to acti-vate the primary task-set during the critical period pre-ceding the primary task goal (9, 1, 2...) during theDART because the dual-task requirements places extrademands on sustained attention resources. Previously,we have demonstrated that TBI patients, during theSART, fail to desychronize alpha power during theupcoming period before the ‘3’ suggesting a decrementin alert responding compared to healthy controls(Dockree et al. 2004). The greater demand of the DARTmay further challenge an already-taxed sustainedattention system in TBI patients reducing the likelihoodthat the primary task-set is re-activated in a timelyfashion proceeding the turn-over of the number se-quence.

An alternative explanation may be that TBI patientshave a deficit co-ordinating a switch from one type oftask-set to another. There is considerable evidence tosuggest that patients with frontal lesions (Burgess 2000;Shallice and Burgess 1991) and brain-injured patients

(Stablum et al. 1994, 1996) have marked difficultyinhibiting performance on one task in order to switch toan intended task. Thus, patients may be unable to dis-engage from the grey target detection and, as a result,neglect the primary task-set. A task-switching deficitmay be independent or additive to a deficit in alertresponding. In the context of a model of alertness pro-posed by Sturm and colleagues, the anterior cingulate(AC) acts to coordinate attentional control. Since theAC is robustly activated under dual-task conditions(Kondo et al. 2004), the dual-task SART may challengean additional node in the sustained attention networkand functional imaging could test this conjecture.

We also acknowledge that the TBI patients may beless able than controls to utilize the turnover of the digitsequence as a cue for the upcoming no-go target. Thiscould reflect a deficit in strategy application which asregularly be observed in TBI patients (Burgess 2000;Levine et al. 2000). However, utilisation of the numbersequence is equally available during the SART andDART suggesting that strategy application does notunderlie the within-subject error differences in the TBIgroup. To test the possibility that emotional differencesbetween the TBI patients and controls were influencingerrors we correlated SART and DART errors with theHAD-anxiety and HAD-depression scores. There wasno strong evidence that higher levels of reporteddepression and anxiety in the TBI group were related tohigher error rates. However, a non-significant trendsuggested that higher anxiety levels in the TBI groupwere related to greater commission errors on the DART.The absence of this trend for HAD-anxiety and SARTerrors might suggest that levels of anxiety become morerelatable under conditions of higher challenge and aretherefore less likely to be an important factor, in general,under low-demand endogenous conditions.

Response time variability (CofV) was associated withhigher error rates on the DART in Experiment 1 withhealthy subjects and in Experiment 2, only for TBI pa-tients. The lower number and range of errors in thesecond group of healthy subjects may explain the ab-sence of the DART-CofV relationship. We alsoacknowledge that the longer trial duration in the mod-ified DART in Experiment 2 may be responsible for this.Nevertheless, TBI patients exhibited significantly greatervariability in their go-trial RTs than controls and thiswas associated with more errors on the DART. Thesefindings replicate and extend those of Manly and col-leagues (Manly et al. 2000) confirming that intra-indi-vidual variability is a strong predictor of sustainedattention performance. Stuss et al. (1999) have alsoshown that impaired attentional control is accompaniedwith increased variability in TBI patients. Further workof Stuss and colleagues suggested that focal braindamage (bilateral dorsolateral prefrontal cortex andsuperior medial frontal areas) rather than brain injuryper se, underlies increased intra-individual variability(Stuss et al. 2003). These findings suggest that dorso-lateral prefrontal activation seen during the SART

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(Manly et al. 2003) may, in part, be responsible forcontrolling variability of alert responding and brain in-jury may disrupt this function.

One of our key reasons for developing the DART isthat during sustained attention to a monotonous goal,an individual will be susceptible to ‘capture’ by com-peting distractors. These will vary with the individualand environment and will be an uncontrolled factorduring the task. However, attempting to constrain dis-traction by including ‘‘built-in’’ distractors may increasethe sensitivity of measuring sustained attention deficits.We argue that the grey items during the DART serve ascontrolled distractors that reduce inadvertent capture byuncontrolled variables allowing primary task monitor-ing to be measured with greater sensitivity. In support ofthis conjecture, we find that response variability is sig-nificantly reduced on the DART compared to theSART. Thus, the additional grey detection requirementof the DART may help to constrain response variabilitykeeping subjects ‘on-task’ under conditions of monot-ony and indexing fluctuations in sustained attentionprocesses more directly. By contrast, during the SART,greater distraction from extraneous variables mayheighten response variability and the CofV will be apoorer reflection of fluctuations in sustained attentionprocesses.

In conclusion, the development of a dual-task sus-tained attention measure proved useful for examiningindividual differences in alert-responding in neurologi-cally healthy adults, and its relationship to everydayattentional failure. We argue that TBI patients showeddifficulties maintaining alert responding during the taskand may also be impaired switching from one task-set toanother. Consequently, sustained attention deficits andadditional executive deficits may have resulted fromtheir brain injury. The findings support and extendprevious work suggesting that heightened response var-iability is associated with increased error rates in TBIpatients. We propose that the DART may be moresensitive to sustained attention deficits in healthy andbrain-injured populations and serve as a laboratoryanalogue to everyday attentional failure.

Acknowledgements We would like to thank all those from theNational Rehabilitation Hospital, Dun Laoghaire, who partici-pated in this research. The Government of Ireland’s Higher Edu-cation Authority supported this research. This work was supportedby a grant from the Irish Higher Education Authority’s Pro-gramme for Research in Third-Level Institutions (8AA. G03007) toProfessor Ian Robertson

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