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Reaction Time Indicators of Attention Deficits inClosed Head InjuryTheodore P. Zahn & Allan F. MirskyPublished online: 09 Aug 2010.

To cite this article: Theodore P. Zahn & Allan F. Mirsky (1999) Reaction Time Indicators of Attention Deficits in ClosedHead Injury, Journal of Clinical and Experimental Neuropsychology, 21:3, 352-367, DOI: 10.1076/jcen.21.3.352.924

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* We thank the Maryland Head Injury foundation for assistance in recruiting participants, Barbara Jones andEdward Turner for clinical evaluation of patients, and Thalene Mallus for expert technical assistance.Address correspondence to: Theodore P. Zahn, Laboratory of Brain and Cognition, National Institute of MentalHealth, Building 10, Room 4C104, 10 Center Drive, MSC 1366, Bethesda, MD 20892-1366, USA. E-mail:ted_zahn@nih.govAccepted for publication: March 19, 1999.

Journal of Clinical and Experimental Neuropsychology 1380-3395/99/2103-352$15.001999, Vol. 21, No. 3, pp. 352-367 © Swets & Zeitlinger

Reaction Time Indicators of Attention Deficits in ClosedHead Injury*

Theodore P. Zahn and Allan F. MirskySection on Clinical and Experimental Neuropsychology, Laboratory of Brain and Cognition, National Institute

of Mental Health, Bethesda, MD

ABSTRACT

The nature of deficits in attention in closed head injury (CHI) was studied by three reaction time (RT)paradigms given to 20 patients who had a CHI 2 or more years previously and to 25 controls. We studiedthe effects of temporal uncertainty by varying the length and regularity of the preparatory interval, theeffects of stimulus modality uncertainty on simple RT to tones and lights, and the effects of responseselection in choice RT. The CHI group showed slower and more variable RT than controls under all condi-tions. In addition, a long preparatory interval on the preceding trial retarded RT more in the CHI group, andthey showed greater effects of stimulus modality uncertainty. Both of these findings suggest a difficulty inshifting attention to unexpected stimuli. These greater effects on RT of variations of attention or prepara-tion in CHI may account for their greater within-subject variability possibly due to frontal lobe damage.

Although impaired attention and concentrationis a frequent clinical complaint of persons whohave suffered closed head injuries (CHI), evenlong after the acute stage, precise empiricalcharacterization of which aspects of attentionare impaired remains elusive. A prominent andconsistent feature of such cases is retarded mo-tor activity as manifested in slow reaction time(RT). However, slow RT is a very nonspecificmarker which does not, by itself, indicate a par-ticular type of attention impairment or if there isan attention problem at all. Therefore proce-dures which are designed to evaluate specificaspects of attention have been used in investiga-tions of CHI.

An hypothesis to explain this generalizedslowing, based on neuropsychological studies, isthat persons with CHI are impaired on con-trolled information processing (Van Zomeren,Brouwer, & Deelman, 1984). This has led to

investigations of the process of slowing usingstage analysis (Smith, 1968; Sternberg, 1969) inwhich various stages of processing are isolatedby experimental manipulation of the parametersof the protocol. For example, in choice RT thenumber of stimulus alternatives (sometimes re-ferred to as ‘complexity’) and stimulus-response(S-R) compatibility are taken to influence thestages of decision-making and response selec-tion, and stimulus similarity to index the stimu-lus encoding stage. In studies using this ap-proach the most consistent finding is a generalslowing in CHI; there is a lack of a consensus ofwhich specific stages are impaired (Van Zome-ren & Brouwer, 1994). Indeed, one comprehen-sive study found retarded RT in CHI but no dif-ferential effects in any single stage (Stokx &Gaillard, 1986). More detailed consideration ofthese points will be presented in the relevantindividual studies to be described below. Large

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intraindividual variability of RT in CHI com-pared to controls has also been a consistent find-ing in those studies which have looked at it(Hetherington, Stuss, and Finlayson, 1996), but,like RT level, it has not consistently been asso-ciated differentially with experimental condi-tions. There seems to be room for somewhatdifferent approaches for the study of attention inCHI.

Slow RT also is present in forms of psycho-pathology in which impaired attention has beenimplicated, suchasschizophrenia (Nuechterlein,1977; Rist & Cohen, 1991) and attention deficithyperactivity disorder (Zahn, Kruesi, & Rapo-port, 1991), and high within-subject variabilityin schizophrenia has been reported. Because ofthe lack of specificity with respect to attentionof RT per se, paradigms have been developed tostudy sustained and selective attention in a moresystematic fashion. The present study comparespersons with CHI with controls on three RT par-adigms which have been used to assess variousaspects of attention in psychopathology.

The most usual site of brain damage in CHI isdiffuse axonal or white matter injury in the cere-bral hemispheres and possibly in the brainstem(Stuss & Gow, 1992). This could account forretarded RT by requiring a more circuitous routeof processing between stimulus and response(van Zomeren & Brouwer, 1994). Different as-pects of attention, such as focussing, sustaining,and shifting may depend on the integrity of sep-arate brain regions (Mirsky, Anthony, Duncan,Ahearn, & Kellam, 1991). To the extent thatdamage in these regions occurs in CHI theremay be additional specific deficits elicited bythese paradigms.

EXPERIMENT 1: THE ‘SET INDEX’PARADIGM

In this procedure, designed to study sustainedattention and variations in preparation, simplewarned RT is measured in relation to the lengthand regularity of the preparatory interval (PI –the interval between the warning signal and theimperative stimulus). Three to 6 discrete PIs,ranging from 1 s up to 25 s in some studies, are

presented in a ‘regular’ or constant PI sequenceand in an ‘irregular’ or variable sequence. Typi-cally, RT is shorter when the stimulus is predict-able (i. e., in the regular series), and it is an in-creasing function of PI duration in the regularseries and a decreasing function of the PI in theirregular series. In addition, in the irregular se-ries RT is retarded on trials when the PI on thepreceding trial (preceding PI or PPI) is longerthan the current PI compared to trials on whichthe PPI is equal to or shorter than the PI. In per-sons with psychopathology in which attentiondeficits are prominent symptoms not only is RTretarded overall, but the above-mentioned trendsare larger (Neuchterlein, 1977; Rist & Cohen,1991; Zahn et al., 1991, 1998).

Brain injured persons have been tested withthis paradigm in at least two previous studies.Costa (1962), using PIs of .5, 2 and 8 s, reportedelevated RTs of about 200 ms but somewhatsmaller and even nonsignificant PI effects in agroup of brain damaged patients compared tocontrols. Using PIs of 1 to 25 s Olbrich (1972)found retarded RTs and slightly, but non-significantly, greater PI effects in a brain dam-aged group compared to controls. PPI effectswere present to about the same degree in eachgroup. The experimental groups in both theabove studies consisted of hospitalized patientswith various types of acute cerebral disease orinjury, in most cases focal. One study of CHIcompared RT after a fixed 2 s PI with that aftera variable PI, finding no group x condition inter-action (Stokx & Gaillard, 1986) suggesting nodeficit in preparation. The purpose of Experi-ment 1 was to attempt to replicate the findingsusing the full protocol on persons with CHI whowere in late stages of recovery.

METHOD

ParticipantsThe 20 CHI participants were recruited fromnearby communities with the help of the MarylandHead Injury Foundation. Their mean age was 35.9(SD = 10.6) years, range 22 to 58 years. The lengthof time since the injury ranged from 26 months to28 years (median = 6.0 years), and the reportedlength of the post injury coma was between 1 and

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395 days (median = 12.5 days; the next longestcoma was 90 days, the 75th percentile was 36days, and the 25th percentile was 4.5 days).

The 25 controls (Ctl) were recruited from non-professional NIH employees and the nearby com-munity. They were screened by interview for theabsence of any current or past Axis I diagnoses,head injury, or past or current substance abuse.Their mean age was 30.4(SD = 8.5) years, range18–56. Only 21 controls participated in Experi-ment 1 because of scheduling difficulties.

All participants gave written informed consentfor these tests and were paid for their participationat standard NIH rates.

Apparatus and ProcedureElectrodes were applied to the nonresponding(left) hand and to the right upper arm and left legto measure autonomic activity. Those data will notbe reported here. After a 5-min rest period a simplewarned RT task was given in which participantswere instructed that on each trial an amber warninglight would come on; when they were ready theyshould depress a telegraph key (placed on the armof their chair) and keep it held down until a tone(’beep’) sounded at which time they should releasethe key as quickly as possible. They were told fur-ther that we were measuring how quickly they re-sponded to the beep.

The preparatory interval (PI) was measuredfrom the time the key was depressed to the onset ofthe RT stimulus. When the key was depressed theamber light went out. If the key was released pre-maturely the amber light reappeared and the samePI was restarted with the next key press. The RTstimulus was an 80 db (re .0002 dynes/cm2), 1000Hz tone which was terminated by the key release.The intertrial interval was variable and unpredict-able between 8 and 14 s (M = 11 s).

Prior to this test, on a separate day, two 9-trialseries with regular 4 and 8 s PIs were given whilephysiological variables were being recorded. Thattest was considered as constituting practice trialsfor this one. An additional 4 warmup trials with a2-s PI were given before this test.

A total of 55 trials were given with PIs of 2, 4,and 8 s. On the first 27 trials (Regular Series) thePI was constant for each 9 trial block. After eachof the first 2 blocks, participants were told that thePI would be lengthened and were reminded to con-tinue to respond to the beep as quickly as possible.On the last 28 trials (Irregular Series) the same 3PIs were presented in a pseudo-random sequencesuch that each PI preceded each other PI, includingitself, an equal number of times and the same PIdid not occur more than twice in succession. Be-

fore this series participants were told that some-times there would be a short wait before the beep,sometimes a medium wait, and sometimes a longwait before the beep and that they wouldn’t knowwhat to expect beforehand. They were again re-minded to respond to the beep as quickly as possi-ble.

Data AnalysesThe mean, median, and standard deviation (SD) ofthe RTs for each PI in each series were the basicdata. The first trial from each series was omittedfrom these computations. These were analyzed byGroup (CHI, Ctl) × Condition (Regular PI, Irregu-lar PI) × PI (2 s, 4 s, 8 s) analyses of covariance(ANCOVA), with the last 2 factors being repeatedmeasures and age as the covariate, using BMDPprogram 4V (Dixon, 1992) with equal weighting ofthe cell means. In the case of main effects and in-teractions involving the PI the Huynh-Feldt epsi-lon correction to the degrees of freedom was em-ployed. Because the results for the mean and me-dian were usually similar, those for just the medianwill be presented, but mean data will be presentedif there is a substantive difference from the me-dian. Only overall group differences in within-sub-ject SD will be presented because of difficulties ininterpreting PI effects on this variable. Plannedtests of the simple effects of PI sequence were alsodone in the case of interactions involving that fac-tor and group. For the irregular PI, RTs on trialswhen the PPI was less than, equal to, or greaterthan the PI were compared, and in addition the ef-fects of PPI for each PI were evaluated by a 2 × 3× 3 (Groups × PI × PPI) ANCOVAs.

RESULTS

Although age did not produce significant effectsin the ANCOVAs the results for these will bepresented (rather than ANOVAs) because of thedifference between groups in age.

The overall Group × Condition × PI analysisproduced significant main effects for Group,F(1,38) = 11.88, p < .002 and Condition,F(1,39) = 27.17,p < .0001 and a Condition × PIinteraction,F(2,78) = 24.72,p < .0001, epsilon= .77, but no interactions involving Group. Asseen in Fig. 1, the CHI group had elevated RTsoverall but only minor, if any, differences in theslopes of the curves. The within-subject vari-ability (standard deviation) of RTs was also

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greater in the CHI group,F(1,38) = 8.12,p =.007. Tests of simple effects showed that theCHI group had elevated RTs for each conditionF(1,38) 9.72,p < .004, but there were noGroup × PI interactions.

ANCOVAs on the relationship between PIand PPI (Fig. 2) showed overall main effects forboth PI,F(2,78) = 24.28,p < .0001, epsilon =1.0, and PPI,F(2,78) = 11.42, p < .0001, epsilon= .95, and also trends for interactions betweenGroup and PI,F(2,78) = 2.60,p < .09, epsilon =1.0, and Group × PPI,F(2,38) = 2.62,p < .09,epsilon = .95. However, for RT means theGroup × PPI effect wasF(2,38) = 3.39,p < .05,epsilon = .94. Tests of simple effects of the PPIfor each PI separately showed one significantGroup × PPI effect: for the mean data at the 8 sPI, F(2,78) = 4.41,p < .02, epsilon = .92, but noeffects for median RTs.

Analyses were done on the change in RTwithin each regular series as estimated by theslope of the RTs over trials. Although there wasa significant overall positive slope,F(1,38) =4.12,p < .05, there were no group differences.

DISCUSSION

The results confirm previous studies using thisgeneral paradigm in showing retarded RTs inpersons with brain injury compared to controls,but little difference in the effects of variations inlength and regularity of the PI. Further, the pres-ent results extend those of previous studies byshowing that they apply to patients with closedhead injury after a sufficient period so as to al-low for much recovery of function. We did,however, find that the length of the PPI had adisproportionate effect on the RTs of the CHIgroup, a result that differs from a previous find-ing of no difference by Olbrich (1972). Thatstudy, however, used quite a different range ofPIs (1 s to 25 s) and the overall PPI effect wassmaller and less significant than that obtainedhere.

The data suggest that slowness and variabilityin performance per se are the major lasting se-quelae to brain injury. In this paradigm varia-tions in the PI are intended to assess aspects of

attention, but other processes such as accuracyof time estimation have also been implicated(Niemi & Näätänen, 1981). Specifically, theincrease in RT with PI duration in the regularseries has been attributed to increasing difficultyin sustaining preparation or attention over time(Shakow, 1962) or to difficulty in timing peakpreparation at longer (constant) PIs (Niemi &Näätänen, 1981). The present data suggest thatneither of these functions are seriously impairedin persons with long standing CHI. Althoughvigilance decrements in recent traumatic braininjured patients have been reported (Whyte, Po-lansky, Fleming, Coslett, & Cavallucci (1995),most of the evidence on chronic CHI using avariety of tasks shows that there is no added im-pairment of performance when attention is re-quired to be maintained over longer periods oftime (Van Zomeren & Brouwer, 1994).

In the irregular PI sequence, because the threePIs are equiprobable on each trial, uncertainty isreduced with time during the PI, and preparationshould increase as a function of PI duration. Per-sons with CHI seem to be similar to controls inthe effects of reductions in uncertainty as shownby their similar slopes of the irregular PI curve.

However, RT is also influenced markedly bythe PPI; long PPIs may alter the expectancy ofor the accuracy of timing of the PI on the nexttrial (Niemi & Näätänen, 1981). Their greaterPPI effect suggests that in CHI expectanciesand/or time estimation are more vulnerable todisruption by extraneous influences and/or thattheir RTs are more retarded when preparation isnot optimal. That this effect was significant formean but not median RT suggests that only afew trials were so affected. It is of interest thatconcurrently-recorded electrodermal responsesto the RT stimuli increased markedly with in-creases in the PPI in controls but only minimallyin the CHI group (Zahn & Mirsky, in press).This suggests that their disproportionately re-tarded RT under those conditions was not due todifferences in expectancies but to less mobiliza-tion of activation.

Brain-injured patients are clearly distinguish-able on this paradigm from persons with schizo-phrenia and attention deficit hyperactivity disor-der who show exaggerated PI effects in addition

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Fig. 1. Median reaction time in relation to the length of the preparatory interval for regular (Reg) and irregular(Irreg) series in participants with closed head injuries (CHI) and controls for Experiment 1.

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ATTENTION IN CLOSED HEAD INJURY 357

Fig. 2. Mean reaction time for each preparatory interval (PI) in relation to the length of the preceding prepara-tory interval in the irregular series in participants with closed head injuries (CHI) and controls for Ex-periment 1.

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to elevated RT (Neuchterlein, 1977; Rist & Co-hen, 1991; Zahn et al., 1991). The present datashow that large PI effects are not necessary con-sequences of slow and variable RT.

EXPERIMENT 2. SIMPLE RT TO TONESAND LIGHTS

This paradigm assesses the effects on RT ofstimulus modality uncertainty by comparing RTto tones and lights under constant modality andvariable modality conditions. Previous researchhas found that RT is faster under constant mo-dality conditions (Kristofferson, 1967) suggest-ing that persons attend to or prepare optimallyfor stimuli in just one modality at a time so thatRT is retarded when a stimulus occurs in theunattended channel. A larger increment in RTunder variable modality conditions would sug-gest a difficulty in shifting attention betweenmodalities.

Variable modality series can also be analyzedfor sequence effects: RT to a stimulus in onemodality is compared for those trials in whichthe modality on the preceding trial was the same(ipsimodal) or different (crossmodal – Sutton,Hakerem, Zubin, & Portnoy, 1961). In most per-sons RT is, on average, faster after ipsimodalthan after crossmodal sequences, although thiscan be a small and inconsistent effect. Cross-modal retardation is larger and more consistentin persons with schizophrenia (Sutton, et al.,1961; Rist & Cohen, 1991) suggesting that thisindexes attention. Benton, Sutton, Kennedy, &-Brokaw (1962) showed that patients with mixedfocal and diffuse cerebral damage, whose over-all RT deficit was about 40 ms, had a greatercrossmodal retardation than controls for tone-light sequences but not for light-tone sequences.

A third aspect of this paradigm involves mix-ing trials with simultaneous presentation of toneand light in a variable-stimulus sequence. Theo-retically the stimulus uncertainty effect shouldbe reduced on simultaneous trials by allowingthe responder to react to that stimulus for whichpreparation is maximal.

METHOD

ParticipantsThese were the same as in Experiment 1.

Apparatus and ProcedureKey-press RTs were recorded to lights and tones.The response apparatus consisted of two lever-switches, one switch conveniently placed for oper-ation with each hand. In this protocol participantsresponded with only their preferred hand. Tones(1000 Hz) were presented from a speaker placedon the floor in front of and to the left of the partici-pant. The light source was a green electrolumines-cent lamp (Grimes, Urbana, OH) with an adver-tised rise time of 90 s. This lamp is a square panelof which the central 6.25 cm2 was exposed. It wasput inside a hood to attenuate ambient light andplaced at eye-level 125 cm in front of the subject.Tones and lights were of 50 ms duration and hadbeen equated for subjective intensity in a separategroup of normal controls. Stimulus presentationand timing of stimuli and responses (in ms) wasdone by a PDP-11 computer. Intertrial intervalswere random between 3 and 4 s.

The sequence of conditions was as follows: (1)Regular series (Reg1) of 10 tones and 10 lights,each preceded by at least 4 practice trials; (2) aVariable Stimulus (VS) series of 49 trials in whichthe tones and lights were presented in a pseudo-random sequence, the same for all participants.They were told that on each trial a tone or a lightwould occur unpredictably and they were to re-spond as fast as possible to whichever stimulusoccurred; (3) a 55-trial Intersensory Facilitation(IF) procedure which was similar to VS except thaton a third of the trials (18) the light and tone oc-curred simultaneously. Participants were told thatoccasionally the light and tone would come on atthe same time, but that they should still respond tothe double stimulus as quickly as possible; (4) aRegular series (Reg2) of 10 lights and 10 tones.

RESULTS

An overall Group × Conditions × StimulusANCOVA on median RT, covarying age (omit-ting the dual-stimulus trials in IF), showed maineffects for Group,F(1,38) = 9.92,p < .004, andCondition,F(3,117) = 97.7,p < .0001, epsilon =.91, and a marginal effect for stimulus,F(1,39)= 3.90,p < .06. More importantly, there was aninteraction of Group and Condition,F(3,117) =

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3.91,p < .02, epsilon = .91, reflecting a greaterincrement in RT for the two variable stimulusconditions in the CHI group (Fig. 3). In additionthere was a Stimulus × Condition interaction,F(3,117) = 4.86,p < .004, epsilon = .79, reflect-ing mainly the large tone advantage for the Regseries and the reversal in the VS condition (Fig.3), but this did not interact with groups. Plannedcontrasts with the combined Reg means pro-duced significant Group × Condition effects forboth VS and IF,F(1,39) = 7.00 & 5.51,p < .02& .03, respectively.

The within-series variability (SD) was alsolarger in the CHI group,F(1,38) = 5.77,p < .03.Although there were robust effects of Condi-tions on the SDs,F(3,117) = 8.72,p < .0002,epsilon = .75, there were no group differences inthese.

For the VS condition there were only mar-ginal effects for Sequence (crossmodal vsipsimodal),F(1,39) = 3.67,p < .07, Sequence ×Stimulus,F(1,39) = 3.89,p < .06, and Group ×Sequence × Stimulus,F(1,39) = 3.50,p < .07.These reflected trends for ipsimodal RTs to befaster than crossmodal RTs, especially when thetone was the stimulus, and that the latter effecttended to be greater in the CHI group.

For the IF condition, RTs to single stimuliwere compared when the preceding trial had thesame or opposite single stimulus or if it was adual stimulus. This analysis showed a very sig-nificant effect of sequence,F(2,78) = 8.61,p =.0004, epsilon = 1.0, reflecting a large cross-modal vs ipsimodal contrast,F(1,39) = 22.5,p <.0001. When the preceding trial had a doublestimulus, RT was intermediate, slower than thaton ipsimodal trials,F(1,39) = 4.20,p < .05, andmarginally faster than that on crossmodal trials,F(1,39) = 3.52,p < .07. Neither Group nor Stim-ulus interacted with Sequence effects.

RT was faster to the simultaneous tone andlight than to either stimulus presented singly inthe IF condition,F(2,78) = 83.9,p < .0001.However, RT to the double stimulus was slowerthan the combined Regular RT to the tone,F(1,39) = 4.75,p < .04, but no different fromthat to the light. There were no interactions withGroup in these analyses. The stimulus on the

preceding trial had no significant effect on RT tothe dual stimuli.

DISCUSSION

For subjects as a whole, RT was greatly retardedby stimulus modality uncertainty compared tothat in both a constant stimulus condition andwhen the tone and light were unpredictably pre-sented simultaneously. In addition analyses ofsequence effects showed an ipsimodal advantagein both variable stimulus conditions althoughthis reached full significance only for the condi-tion that also included double stimuli (IF). Thusthe paradigm reproduced results found in previ-ous studies.

The CHI group had very prolonged and vari-able RT under all conditions compared to con-trols. They also showed greater slowing, com-pared to controls, from stimulus modality uncer-tainty in comparison with the constant-stimulusconditions. To our knowledge no previous studyhas investigated this in brain-injured persons.The retardation due to stimulus uncertainty con-firms the hypothesis that maximal preparation ispossible for stimuli in only one modality at atime. In an uncertain stimulus condition thestimulus actually presented will not be the oneprepared for on about half of the trials and atten-tion will have to shift to the other modality.Thus the added increment in RT for the CHIgroup compared to the controls is evidence thatbrain injury slows the attentional shift process.Whether this deficit is specific to shifting atten-tion between modalities, and indeed whether itextends to other modalities, cannot be answeredby this study. Shum, McFarland, Bain, & Hum-phreys (1990) postulated a defect in the stimulusidentification stage of processing in patientswith severe brain injuries tested soon after theirinjury who had overall RT impairments similarto that seen here. The present data might bethought similarly to indicate slow stimulus iden-tification in CHI. However Shum’s finding wasbased on variations in stimulus proximity in aspatial choice RT task, a quite different opera-tion than used here.

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Fig. 3. Median reaction time to tones (TN) and lights (LT) in participants with closed head injuries (CHI) andcontrols (CTL) under 5 conditions of Experiment 2. VAR STIM = variable stimulus; INTER FACIL =intersensory facilitation.

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Under the attentional shift hypothesis, a dis-proportionate speeding with simultaneous stim-uli and crossmodal retardation might also beexpected in CHI. There were nonsignificantgroup differences in the expected direction forimprovement in RT with double stimuli in the IFcondition as well as for crossmodal retardationin the CHI group for RTs to tones in the VS con-dition. These two marginal results provide addi-tional, if weak, confirmation of an attentionalshift deficit in CHI. Fewer trials contributed tothe dual stimulus and crossmodal retardationeffects than to the comparison of the Reg andVS conditions. This should increase the varianceand attenuate the significance of the difference.In addition, the crossmodal retardation effectmay be attenuated by individual differences inthe extent to which expectancy or preparation isenhanced by a similar stimulus on the precedingtrial. Some persons on some trials might expecta modality shift. Our crossmodal result partiallyconfirms the greater crossmodal retardation bybrain-damaged patients compared to controlsreported by Benton et al. (1962) except that theyobserved this only in RTs to lights. Their patientgroup contained few, if any, CHI cases and so isnot comparable to the present sample

Studies of schizophrenia (Kristofferson,1967; Zahn et al., 1997) and ADHD (Zahn et al.,1991) have found significant or marginal effectsfor modality uncertainty but not for crossmodalretardation. Thus the VS – Reg comparisonseems to be more sensitive to attention impair-ments than the crossmodal effect.

On the basis of studies using the WisconsinCard Sorting Test (WCST) in schizophrenia,deficits in shifting attention are thought to re-flect impairment in frontal lobe function(Weinberger, Berman & Zec, 1986; Mirsky etal., 1991). Patients with CHI have been shownto have ‘frontal’ symptoms and deficits includ-ing impaired WCST shift performance (Stuss &Gow, 1992). Although the attention shift deficitshown by the CHI group in this study is opera-tionally different from those indexed by theWCST, it still may be mediated by specific fron-tal pathology in these patients in addition to theaxonal damage.

EXPERIMENT 3. CHOICE RT AND SEN-SORY DOMINANCE

The purpose of this paradigm was first, to studythe effects of adding a response-selection stageto the modality uncertainty condition, second, tostudy crossmodal vs ipsimodal sequences inchoice RT, and third, to study sensory domi-nance. RTs to lights and tones were recordedunder 3 conditions similar to those used in Ex-periment 2 except that participants responded tothe tones and lights with different hands. TheRegular conditions consisted of all tones or alllights; the tones were responded to with onehand and lights with the other. In a choice RTcondition, the tones and lights were presentedrandomly. In a sensory dominance (SDom) pro-cedure, the two stimuli were again presentedrandomly, but on a third of the trials the toneand light occurred simultaneously and the sub-ject was instructed to respond toeach stimulusas quickly as possible.

The hypothesis of retarded information pro-cessing in CHI would predict an increasing defi-cit with increasing task complexity, which isindexed by the number of alternatives in achoice RT task (Van Zomeren & Brouwer,1994). A meta-analysis of studies which variedtask complexity in patients in their first year ofrecovery produced partial support for this hy-pothesis (Van Zomeren & Brouwer, 1994), butonly when task complexity was great enough toproduce RTs of 700 ms or more in control sub-jects. With tasks producing RTs of 200 – 500ms, there seems to have been an equal elevationin RT in CHI and control groups.

Other studies have indexed response selectionby varying stimulus-response (S-R) compatibil-ity in a choice reaction time task. Greater effectsof S-R compatibility in CHI have been reported(Shum et al., 1990; Schmitter-Edgecombe,Marks, Fahey, & Long, 1992), even in onegroup without significantly elevated overall RT(Shum et al., 1990). However, Stokx andGaillard (1986) had previously failed to find adifferential effect of S-R compatibility in a braininjured group despite slower RT overall in pa-tients than in controls. These studies did not in-clude a simple RT condition. Because in the

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present setup the speaker for the tone was inad-vertently placed to the left of center (the lightbeing straight ahead), and alternate participantsreceived each stimulus-response mapping (tone– left hand, light – left hand), S-R compatibilityeffects can be tested.

Crossmodal retardation in schizophrenia hassometimes been studied within a choice RT par-adigm although less frequently than with simpleRT. Similar, but less consistent findings as thoseobtained with simple RT have been reported(Rist & Cohen, 1991; Zahn et al., 1998). To ourknowledge this paradigm has not been used instudies of brain injury.

When lights and tones are matched in subjec-tive intensity under regular conditions RT totones is typically faster than that to lights; thetone advantage disappears in choice RT, andwhen the stimuli are occasionally presented si-multaneously, RT to lights is faster (Colavita,1974; Egeth & Sager, 1977). These results havesuggested that humans typically show visualdominance – that is, by default, attention is di-rected toward vision rather than audition.Posner, Nissen, and Klein (1976) speculated thatthis may be due to the low alerting capacity ofvisual stimuli which produces a compensatoryvisual attentional bias. That visual perceptionusually entails orienting the eyes may also playa role here. This procedure has not been used tostudy brain injury previously. It might be specu-lated that deficits in attention would disrupt thisprocess.

METHOD

ParticipantsThese were the same as in the prior experimentsexcept that all 25 of the controls participated inthis one.

Apparatus and ProcedureThe apparatus was the same as that used in Experi-ment 2, but both response keys were used. Alter-nate participants responded with right hand totone, left to light; the remainder got the conversemapping of stimuli to hand. The mapping remainedthe same for tests on each treatment. The condi-tions were as follows: (a) Regular series of 10

tones and 10 lights each preceded by at least 4practice trials (Reg 1); (b) 49 Choice RT trials inwhich the tones and lights were presented in apseudo-random sequence, the same for all partici-pants; (c) a 55-trial sensory dominance (SDom)procedure which was similar to Choice RT exceptthat on a third of the trials the light and tone oc-curred simultaneously (SDom-Double); and (d) afinal Regular series of 10 lights and 10 tones (Reg2). In the SDom procedure participants were toldthat occasionally the light and tone would come onat about the same time, and on those trials theyshould respond toeach stimulus as quickly as pos-sible. This phrasing was carefully chosen on thebasis of pilot work to encourage separate respond-ing to the two stimuli – i. e., to discourage simulta-neous responding. The intertrial interval was ran-dom between 3 and 4 s for each condition.

RESULTS

There were no group differences in errors or innonresponses (RTs exceeding the 2 s upper cut-off). Participants with the incompatible mapping(light – left hand) had more errors on bothChoice and SD Single,F(1,41) = 7.27,p = .01,but there were no interactions with group or dif-ferences between conditions.

Figure 4 shows the overall results for the 4conditions, with the SD Sing and SD Doubshown separately. In the Group × Mapping ×Condition × Stimulus ANCOVA there were sig-nificant main effects for Group for both medians,F(1,40) = 10.8,p < .003 and within-subject SDs,F(1,40) = 7.84,p < .008, and no interactions withconditions. A Condition × Stimulus effect,F(4,64) = 16.5,p < .0001, epsilon = .71, re-flected the faster RT to tones in the Reg condi-tions, but faster RT to light in all other condi-tions especially in the SD Doub condition. This,in turn, interacted with Mapping,F(4,164) =6.36,p < .0006, epsilon = .71. There was also amarginal 4-way interaction, which includedgroup,F(4,164) = 2.52,p < .07, epsilon = .71.This was due to the 3-way interaction just in theCHI group,F(4,164) = 7.34,p < .0002, epsilon =.71, reflecting that the condition × stimulus ef-fect was stronger for the compatible tone – lefthand mapping due to a large light advantage inthe SD Doub for the tone – left subgroup (Fig. 4).

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ATTENTION IN CLOSED HEAD INJURY 363

Fig. 4. Median reaction time to tones (TN) and lights (LT) in participants with closed head injuries (CHI) andcontrols (CTL) under 5 conditions of Experiment 3. Separate curves are presented for the stimulus-response mapping conditions of tone – left hand (TL) and light – left hand (LL). Note REG = Regular;SD = Sensory Dominance; SING = single stimuli; DOUB = double stimuli.

Tests of simple effects for each conditionshowed, rather paradoxically, that although thegroup effect was significant for each condition,it was more so in both Reg conditions,F(1,40)19.8,p .0001, than in any of the irregular con-ditions for which Choice was the most signifi-cant,F(1,40) = 8.05,p < .007. The stimulus ef-fects were reliable for each of the conditions atp < .02 or better. However in the SD Doub con-dition there was a Stimulus × Map interaction,F(1,41) = 6.93,p < .02 and a marginal Group ×Stimulus × Map effect,F(1,41) = 3.53,p < .07,showing the effect of mapping in the CHI group

as indicated above. Planned contrasts betweenthe pooled regular conditions and each othercondition showed a significant Condition ×Stimulus term significant atp = .0004 or betterand a contrast between SD Sing and SD Doubproduced a Condition × Stimulus interaction atp < .01. Thus the subjects as a whole showedvisual dominance under conditions of stimulusuncertainty, and this was maximal for the SDDoub condition. The only group difference in allthis was the aforementioned greater visual domi-nance effect for SD Doub for the CHI subgroupwho had the compatible mapping.

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364 TH. P. ZAHN AND A.F. MIRSKY

In the choice RT condition RT after cross-modal sequences was, surprisingly, faster thanthat after ipsimodal sequences,F(1,41) = 5.65,p< .03. This did not interact with group, but sepa-rate analyses for each group showed a signifi-cant sequence effect only for the controls (p <.04). There was a Sequence × Stimulus × Map-ping × Group effect,F(1,41) = 6.90,p < .02,based on a Sequence × Stimulus × Mapping ef-fect, F(1,41) = 8.60,p < .006, for just the CHIgroup. This was due to a small ipsimodal facili-tation of RTs to tones and a large crossmodalfacilitation in RTs to lights for the compatibleTone-Left mapping and the converse result forpatients with Light-Left mapping. The controlsshowed modest crossmodal facilitation in all 4conditions.

In the SD condition, when just trials with sin-gle stimuli preceded by single stimuli were con-sidered, there were no sequence differences.However, the RTs to single stimuli were greatlyretarded when these followed a double stimulus,F(2,82) = 37.8,p < .0001, epsilon = 1.0, particu-larly for the less compatible Light-Left mappingas shown by a Sequence × Mapping effect,F(2,82) = 5.20,p < .008, epsilon = 1.0. Therewere no group differences in this. For double-stimulus trials there were no sequence effects.

RT to error trials was compared to RT to tri-als where the response was correct for those par-ticipants who had at least two errors. Only theSD condition produced a large enough samplefor a meaningful analysis (10 CHI and 7 Con-trols). Error RTs were faster than correct RTs asexpected,F(1,15) = 6.37,p < .03, but the groupsdid not differ in this.

DISCUSSION

Although, as in Experiments 1 and 2, the CHIgroup had much slower RT overall than con-trols, there were no simple interactions withconditions. Choice RT was markedly slowerthan Reg RT in both groups and there was a fur-ther increment in RT in the SD conditions. Thepresence of the SD Doub condition may haveacted like a third ’choice’ – responding withboth hands in addition to either hand separately.

Thus the CHI group showed no greater effects ofincreases in task complexity than controls. Infact the group difference in RT was more highlysignificant in the Reg conditions than in othersbecause of smaller within-group variances,probably due to the lack of extraneous sourcesof variation.

Although this result seems to conflict withthose of previous studies showing dispropor-tionately retarded Choice RT in CHI, those stud-ies included more than 2 choices and involvedspatial rather than modality choice. It waspointed out earlier that in choice RT studies theRT deficit in CHI increased only for tasks inwhich RT was > 600 ms (Van Zomeren &Brouwer, 1994), and, in fact, Van Zomeren &Deelman (1976) reported slightly less of a defi-cit in CHI in a 2-choice spatial RT task in whichboth hands were used than in simple RT. Theseauthors reported more of a deficit in CHI pa-tients on 4-choice spatial RT than simple RT asdid Ponsford & Kinsella (1992). Thus the pres-ent task was probably not complex enough toproduce an added deficit in RT in our patients.

Some previous studies have concluded thatthe response selection stage is slowed in CHI onthe basis of larger effects of differences in S-Rcompatibility in CHI compared to controls(Shum et al., 1990; Schmitter-Edgecombe et al.,1992), although there are contradictory findings(Stokx and Gaillard, 1986). The lack of suchdifferential effects here perhaps can be best at-tributed to a very weak overall compatibilityeffect: There were no main effects of S-R map-ping for all the conditions or in the analyses ofthe simple effects for the Choice and SD condi-tions. This is probably due to the compatibilitybeing based on sound localization rather than thevisual localization used in previous studies.

A more difficult question is why the variablestimulus (VS) condition in Experiment 2 pro-duced a larger CHI deficit compared to the Regconditions and Choice did not. Adding a re-sponse selection stage to the stimulus uncer-tainty already present in the VS paradigmshould, if anything, add to the deficit. In fact, itdid, but not significantly; the overall group dif-ference for VS is 89 ms and for Choice it is 95ms, a nonsignificant difference. It is possible

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ATTENTION IN CLOSED HEAD INJURY 365

that the added variance from the response selec-tion stage was enough to render the differencenonsignificant. The averaged standard deviationfor Choice RT was 40% larger than that for VS.Nevertheless, this reasoning does not affect theconclusion that the response selection stage ofprocessing was not affected by CHI.

The results here for both groups replicate pre-vious studies showing visual dominance whichis maximally present during simultaneous pre-sentation of auditory and visual stimuli(Colavita, 1974; Egeth & Sager, 1977). The CHIgroup was not only not impaired on this but thesubgroup with compatible S-R mapping actuallyshowed greater visual dominance than the con-trols. There is no ready explanation for this re-sult, and in the absence of replication it probablyshould be left as a potentially intriguing findingbut possibly due to chance.

GENERAL DISCUSSION

As with much previous research, persons withCHI were very significantly slower and theirRTs were more variable than controls under allconditions, but differential effects of conditionswere infrequent and, when found, relativelysmall. Evaluation of performance deficits inCHI is complicated by the clinical variables ofthe severity of the trauma, as indexed by thelength and severity of the coma or post-trau-matic amnesia, and the length of time since thetrauma. These may be expected to be related tocurrent impairment and hence the likelihood offinding performance deficits. However it may beargued that a more direct measure of currentimpairment is overall slowness since that seemsto be an ubiquitous accompaniment of CHIwhich covaries with the two clinical variables(Van Zomeren & Brouwer, 1994). By thatmarker, the present CHI sample showed definiteevidence of the residual effects of the trauma.This global slowing is consistent with diffuseinjury to cerebral and possibly brainstem whitematter thought to be the primary sequel of CHI(van Zomeren & Brouwer, 1994).

Two differential effects of conditions wereapparent: A greater slowing of RT with longer

PPIs in the variable PI series of Experiment 1and a greater effect of stimulus modality uncer-tainty in Experiment 2. If it is the case that longPPIs bias the time estimation on the subsequenttrial (Niemi & Näätänen, 1981) then preparationto respond at the time of the next stimulus willbe impaired. Similarly, in the VS paradigm thestimulus modalitynot prepared for will occurabout half the time. Thus taking both paradigmstogether the hypothesis seems tenable that thegreater slowness in CHI occurs in responding tounexpected stimuli, either because they occurbefore peak preparation has been attained orbecause a stimulus in the other modality hasbeen prepared for.

This aspect of attention has apparently notbeen studied in CHI using simple tasks. Studiesof divided attention in simulated driving tasks,in which sudden deviations in the course of thesimulated car were interposed during perfor-mance of another task, showed no particular ad-ditional impairment in compensatory behaviorwhich were not present in the single-task situa-tion in CHI cases (Brouwer, Ponds, VanWolffelaar, & Van Zomeren, 1989, Van Zome-ren & Brouwer, 1994). However that task invol-ves highly compatible motor responses to kines-thetic and tactile stimulation which, moreover,may be overlearned in experienced drivers andthus do not require controlled information pro-cessing.

A deficit in responding to stimuli for whichpreparation was not optimal could possibly ex-plain the greater intraindividual variability ofRT in CHI. Momentary lapses of attention orpreparation, which occur in all persons even un-der constant-stimulus conditions, would thushave a greater detrimental effect on the CHIgroup and increase their variability of perfor-mance whether or not they actually had moresuch lapses.

In conclusion, the data from these three ex-periments do not support the hypothesis of ageneral deficit in attention or controlled infor-mation processing in CHI. Rather, they suggestan hypothesis of a specific and particular CHIimpairment in responses to stimuli for whichpreparation is relatively weak. This suggests thatthe process of preparation may be retarded in

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CHI. Preparation presumably entails directingthe focus of attention to a particular sensori-mo-tor sequence and partial organization of the mo-tor response. When this peaks at the time thestimulus is presented, the response to the appro-priate stimulus will be facilitated. If this statehas not been reached at the time of the stimulus,or if an unexpected stimulus occurs, then part ofthis process must take place after stimulus onsetthus delaying responding. If it is assumed thatslowness in CHI is due primarily to lesions inwhite matter, then their retarded responding tounprepared-for stimuli suggests that the processof refocussing and motor reorganization in-volves connections between two or more brainareas. Just what brain areas (besides, of course,sensory and motor areas) are involved in thisprocess are unknown, but it might be supposedthat the sensory-motor sequences established bytask instructions would be held in workingmemory which may involve frontal and perhapshippocampal areas (Goldman-Rakic, 1994). Re-focussing attention may also involve structuresthat have been implicated in support of the ‘fo-cus/execute’ attentional element, i.e. the inferiorparietal lobe, the superior temporal sulcus, andsome of the components of the corpus striatum(Mirsky et al., 1991).

Whatever the neurological substrate, this par-ticular pattern of deficits was unexpected andthus not only requires replication using similarmethods but further testing by methods designedto isolate the critical factors more specifically.

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