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Time discrimination in traumatic brain injurypatientsGiovanna Mioni a , Franca Stablum a & Anna Cantagallo ba Dipartimento di Psicologia Generale, Università di Padova, Padua, Italyb BrainCare, srl, Padua, ItalyVersion of record first published: 24 Dec 2012.

To cite this article: Giovanna Mioni , Franca Stablum & Anna Cantagallo (2012): Time discrimination in traumaticbrain injury patients, Journal of Clinical and Experimental Neuropsychology, DOI:10.1080/13803395.2012.755151

To link to this article: http://dx.doi.org/10.1080/13803395.2012.755151

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JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY2012, iFirst, 1–13

Time discrimination in traumatic brain injury patients

Giovanna Mioni1, Franca Stablum1, and Anna Cantagallo2

1Dipartimento di Psicologia Generale, Università di Padova, Padua, Italy2BrainCare, srl, Padua, Italy

Time management skills are required for most daily activities. Traumatic brain injury (TBI) patients often presentwith cognitive dysfunction, but few studies have investigated temporal impairment. The aim of the present studywas to assess temporal abilities in TBI patients using a time discrimination task. Twenty-seven TBI patients (ages=18–60 years) and 27 controls (ages = 20–60 years) were asked to discriminate between two time intervals presentedsequentially. The standard intervals were 500 ms or 1,300 ms long followed by a comparison stimulus that was25% shorter or longer than the standard one. Participants were also asked to perform two tasks to assess attention,speed-of-processing (the Stroop task), and working memory (the n-back task) abilities. The TBI patients were lessaccurate than the controls on the time discrimination task and showed greater time-order error effects. In fact, TBIpatients pressed the “short” key more times when the standard time interval was 500 ms and the “long” key moretimes when the standard interval was 1,300 ms. Significant correlations were found between time discrimination,working memory, and speed of processing in both TBI and controls when the standard time interval was 1,300 ms.Attention appeared to be involved in different ways in the two groups. Working memory and speed of processingwere involved in time processing only in TBI patients when the standard time interval was 500 ms. These data lendadditional support to the notion that two different systems are responsible for elaborating time durations shorteror longer than a second.

Keywords: Traumatic brain injury; Time discrimination; Attention; Working memory; Speed of processing.

INTRODUCTION

The ability to estimate the passage of time is a keyelement involved in most daily activities; neverthe-less how individuals perceive time is still not entirelyunderstood. Good temporal skills are essential fornormal daily activities such as crossing a busystreet, preparing a meal, or organizing the day’sschedule.

A dominant theory with respect to time per-ception explains temporal judgments made on thebasis of a clock stage, memory stores, and deci-sion mechanisms (scalar-timing model; Church,1984; Gibbon, 1991; Treisman, 1963). The clock

The information in this manuscript and the manuscript itself have never been published either electronically or in print. There areno financial or other relationships that could be interpreted as a conflict of interest affecting this manuscript. This research received nospecific grant from any funding agency, or commercial or not-for-profit organizations. The authors gratefully acknowledge the staff ofthe Modulo di Neuropsicologia Riabilitativa (Azienda Ospedaliero–Universitaria Ferrara, Italy) and the participants and their familiesand friends who cooperated in this study. The authors are grateful to Linda Inverso Moretti for her assistance in editing the Englishversion of this manuscript.

Address correspondence to Giovanna Mioni, Dipartimento di Psicologia Generale, Università di Padova, Via Venezia 8, 35131Padova, Italy (E-mail: giovanna.mioni@unipd.it).

stage consists of a pacemaker (an internal clock), aswitch, and an accumulator. The pacemaker emitspulses at a regular rate. When a temporal dura-tion must be estimated, the switch is turned on,and the accumulator counts the total number ofpulses emitted during that time period. The dura-tion perceived represents the total number of pulsesthat are transferred to a working memory store-house where a comparison with the contents ofthe reference memory is made. The reference mem-ory stores long-term memory representations ofpast temporal information. More recent researchemphasizes the mediation of attention and memoryprocesses involved in temporal judgments. Block

© 2012 Taylor & Francis

http://www.tandfonline.com http://dx.doi.org/10.1080/13803395.2012.755151

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and Zakay’s (1996, 2006) proposal is based on thescalar-timing model but also incorporates a cog-nitive module in the form of an attentional gate,which explains the influence of attentional resourceallocation on temporal judgments. The model pre-dicts that participants with attention and workingmemory problems should make more timing errorswith respect to those with more efficient controlfunctions (Pouthas & Perbal, 2004; Zakay & Block,1996, 2004).

There are four major experimental methods forassessing the accuracy of temporal processing:time reproduction, time production, verbal estima-tion, and method of comparison (Block, Zakay,& Hancock, 1998; Grondin, 2010; Zakay, 1990).In time reproduction tasks, participants must repro-duce the duration of a previously presented stimu-lus. The time interval presented needs to be encodedand stored in the reference memory from whichit will subsequently be retrieved and reproduced(Block & Zakay, 2006; Buhusi & Meck, 2005;Grondin, 2010). In time production tasks, partici-pants are required to produce a time interval and totranslate it from an objectively labeled duration toa subjectively experienced one. In verbal estimationtasks, participants are exposed to a time intervaland are then required to translate it (objective dura-tion) into clock units (subjective duration; Buhusi &Meck, 2005; Grondin, 2010). Time production andverbal estimation are suitable methods to investi-gate the rate of the internal pacemaker (Block et al.,1998; Meck, 1996; Rammsayer, Hennig, Haag, &Lange, 2001).

A time discrimination task, one of the most fre-quently used temporal comparison tasks (Grondin,2010; Rubia, Taylor, Taylor, & Sergeant, 1999), wasemployed in the present study. In time discrimina-tion tasks, participants are asked to judge the rela-tive duration of two sequentially presented intervals(a standard time interval and a comparison one)and to indicate whether the second stimulus isshorter or longer than the first one (Grondin, 2010).Temporal performance is modulated by stimulusduration and by the magnitude of the time dif-ference between the two stimuli; the greater thedifference between the two stimuli the higher theaccuracy tends to be (Grondin, 2010). Temporalperformance is, moreover, modulated by the orderin which the standard and comparison stimuli arepresented (Le Dantec et al., 2007; Paul, Le Dantec,Bernard, Lalonde, & Rebaï, 2003). Order of presen-tation of standard and comparison stimuli can varyfrom trial to trial (roving method; Grondin, 2010;Macmillan & Creelman, 2005) or can always be pre-sented in the same order with the standard stimulusbeing presented first followed by the comparison

one (reminder method; Grondin, 2010; Grondin &McAuley, 2009). In both methods, presenting twointervals one after the other induces a bias in per-ceiving the duration, often called time-order error(TOE; Hellström, 1985; Hellström & Rammsayer,2004). Generally, when standard time intervals varywithin the same session, TOE has been found tobe negative for longer durations (the comparisonintervals are perceived as being longer than thestandard intervals) and positive for shorter ones(the comparison intervals are perceived shorterthan the standard ones; Hellström & Rammsayer,2004).

Some authors have speculated that time dis-crimination is the purest measure of time per-ception (Rubia et al., 1999) and, compared totime reproduction and time production, it appearsto be the best method to detect temporal dif-ferences when short intervals (from hundreds ofmilliseconds to a few seconds) are employed(Rammsayer, 2001). Time discrimination perfor-mance predominately relies upon working mem-ory abilities, as participants must bear in mindthe initial time interval while simultaneously pro-cessing another comparison one. Adequate atten-tion and speed-of-processing capacities are, more-over, required to accurately discriminate betweentwo temporal stimuli and to rapidly respond afterthe second stimulus has been presented (Grondin,2010).

Time perception relies on various cognitive pro-cesses such as attention, working memory, andspeed of processing (Block & Zakay, 1996), allconnected to frontal lobe functioning (Moscovitch,1995; Shimamura, 1995). Given the vulnerabil-ity of the frontal lobes to damage as a resultof traumatic brain injury (TBI; Aharon Peretz &Tomer, 2007; Bigler, 2001, 2007) and in view of thefact that cognitive dysfunction commonly followsTBI (Boelen, Spikman, Rietveld, & Fasotti, 2009;Hartikainen et al., 2010), it would seem reason-able to expect time perception alteration in thesepatients. Temporal dysfunctions have, in fact, beendocumented in patients with focal frontal lesions(Casini & Ivry, 1999; Harrington, Haaland, &Knight, 1998; Mangels, Ivry, & Shimizu, 1998;Nichelli, Clark, Hollnagel, & Grafman, 1995;Picton, Stuss, Shallice, Alexander, & Gillingham,2006; Rubia & Smith, 2004).

To our knowledge, only five studies have inves-tigated time perception abilities in TBI patients(Anderson & Schmitter-Edgecombe, 2011; Meyers& Levin, 1992; Mioni, Stablum, McClintock, &Cantagallo, 2012; Perbal, Couillet, Azouzi, &Pouthas, 2003; Schmitter-Edgecombe & Rueda,2008; Table 1).

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TIME DISCRIMINATION AFTER TBI 3

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Three of these were conducted using time repro-duction tasks (Meyers & Levin, 1992; Mioni et al.,2012; Perbal, Couillet, Azouzi, & Pouthas, 2003),one (Perbal et al., 2003) also utilized a time produc-tion task, while three used time verbal estimationtasks (Anderson & Schmitter-Edgecombe, 2011;Meyers & Levin, 1992; Schmitter-Edgecombe &Rueda, 2008). All five studies used time durationsfalling within a range between 4 and 60 s, andall found temporal dysfunction when TBI patientswere tested using long intervals, which probablyexceed the episodic memory span (Meyers & Levin,1992; Schmitter-Edgecombe & Rueda, 2008). TBIpatients were, moreover, more variable in their per-formance with respect to healthy controls, and thishas been linked to working memory and atten-tional dysfunction (Mioni et al., 2012; Perbal et al.,2003).

It should be noted that the literature on timeperception in frontal lobe patients shows tempo-ral dysfunction even when they are exposed totime intervals in the seconds and milliseconds range(Casini & Ivry, 1999; Harrington et al., 1998;Nichelli et al., 1995; Picton et al., 2006; Rubia &Smith, 2004;). As TBI and frontal patients maypresent lesions in similar brain regions and havesimilar cognitive dysfunctions (Knight, Harnett, &Titov, 2005), we expected to find temporal dysfunc-tion even when TBI patients are tested using timedurations falling in the milliseconds and secondsrange.

To date, despite the fact that numerous every-day activities fall within a time range of millisec-onds to a few seconds (Block, 1990; Buhusi &Meck, 2005; Fraisse, 1984), no studies have inves-tigated temporal abilities in TBI patients usingthose intervals. We predicted that TBI patientswill present temporal dysfunction even when testedusing durations ranging from hundreds of millisec-onds to few seconds. A difference in temporal per-formance, with reference to time intervals shorteror longer than 1 second, is another important sub-ject needing investigation. In accordance with thehypothesis that there are two distinct timing mech-anisms (more automatic for the milliseconds rangevs. more controlled for the seconds range; Lewis& Miall, 2003a, 2003b), we predicted higher cogni-tive involvement when participants are required todiscriminate longer time intervals.

One of the novelties about this research liesin the attempt to further investigate the relation-ship between standard and comparison intervalsby analyzing the number of keys pressed. Thisdependent variable makes it possible to quantifythe response bias. If only accuracy had been takeninto consideration, information concerning the type

of errors made by the participants would havegone unnoticed. Participants in the present studywere required to discriminate between two tempo-ral intervals by pressing two distinct keys. As anequal number of accurate responses are connectedto each key, a larger number of key presses oneither side could indicate a response bias, whichis often observed (Hellström, 1985; Hellström &Rammsayer, 2004) but has never been investigatedin TBI patients.

METHOD

Participants

Twenty-seven TBI patients (8 females and 19 males)took part in the study. The patients’ demographicand clinical features are outlined in Table 2.The TBI patients were all right-handed, weretested at least 6 months after their injury, andhad a score equal to or above 6 on the Levelof Cognitive Functioning (LCF) scale (Hagen,Malkmus, Durham, & Bowman, 1979). The LCFscale is used to assess cognitive functioning inpostcoma patients (a score = 6 is the prerequi-site for TBI patients to be tested and indicatesthat patient gives appropriate responses in famil-iar contexts but may still have memory problems).All the patients were able to provide neuroimaginginformation (computed tomography or magneticresonance imaging) showing damage to a varietyof cortical areas, and the majority had frontallesions. According to available clinical records, theparticipants were not densely amnesic or aphasic.Patients who had preexisting neurological, psychi-atric, or developmental disorders, a history of sub-stance or alcohol abuse, or previous head injurywere excluded. This study was conducted in accor-dance with the principles of the Declaration ofHelsinki, and all the patients and participants gaveinformed consent (59th WMA General Assembly,Seoul, 2008).

The control group was made up of 27 par-ticipants matched for gender, age, and level ofeducation (8 females and 19 males; mean age =36.37 years, SD = 9.20, range = 20–60; mean levelof education = 11.74 years, SD = 4.11, range =8–18). All were recruited through the University ofPadua or the community, the controls were right-handed, had never suffered from TBI, and hadno neuropsychiatric disorders or history of drug-alcohol abuse. The differences in age, t(52) = 0.229,p = .820, d = 0.06, or level of education, t(52) =−0.89, p = .375, d = –0.24, between the TBI andthe control group were not significant.

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TABLE 2Demographic and clinical features of the TBI patients

Patient Gender Age Education Cause Injury site PTA GCS TPI LCF FIM/FAM

1 M 49 13 car F bilateral 90 11 18 7 932 M 19 8 car F-T right NA 3 7 7 903 M 47 11 car F bilateral 24 3 50 7 794 F 36 18 fall F 120 6 49 8 815 M 46 7 car F NA NA 15 6 866 M 42 18 bicycle F-T left 35 10 6 7 967 M 18 8 car DAD 28 5 6 7 958 M 22 8 car DAD NA NA 20 6 909 M 32 8 car F bilateral 42 NA 14 6 8610 F 44 13 car F bilateral NA 8 26 7 9311 F 46 13 fall F NA 15 24 6 8312 F 60 5 fall F 24 NA 24 6 8513 F 18 8 bicycle DAD 28 NA 7 6 8714 M 28 8 car F-P left NA 6 34 6 8615 F 41 18 car DAD NA NA 21 6 8616 M 58 18 MB F bilateral 30 9 6 6 9717 M 31 8 car F right 120 NA 80 6 8218 M 32 8 car F bilateral NA 6 108 8 9519 M 28 13 car F-P left 112 NA 60 6 7220 M 50 8 car F-P left 150 NA 90 6 6721 M 43 8 car F-T left NA 4 60 7 8622 F 42 8 car F-T left 35 5 21 7 8323 M 31 16 MB DAD 90 4 12 6 8624 F 33 8 car F-T right NA 15 15 6 7425 M 50 5 car F-P right 35 3 6 7 8226 M 34 13 car F right 42 6 10 7 9427 M 20 13 car DAD NA NA 25 8 82

Mean (SD) 37.04 10.74 car 70% frontal 83% 62.81 7 30.15 6.59 85.78(11.98) (4.11) (43.00) (3.84) (27.78) (0.69) (7.38)

Note. TBI = traumatic brain injury. M = male; F = female. Cause referred to the cause of accident; MB = motor-bike. Injury sitereferred to the prevalent site of injury; F = frontal; F-T = frontotemporal; F-P = frontoparietal; DAD = diffuse axonal damage. NA =not available. PTA = posttraumatic amnesia (days); GCS = Glasgow Coma Scale (Teasdale & Jennett, 1974); TPI = time post injury(months); LCF = level of cognitive functioning (Hagen, Malkmus, Durham, & Bowman, 1979); FIM/FAM = functional independencemeasure/functional assessment measure (Hall, Hamilton, Gordon, & Zasler, 1993).

Procedure

All the patients were recruited and tested at theModulo di Neuropsicologia Riabilitativa (Ferrara,Italy), while controls, who were individuals whoresponded to an advertisement, underwent testingat the Department of General Psychology (Padua,Italy). During the tasks the participants were seatedat a distance of approximately 60 cm in front of a15′′ PC monitor screen. E-Prime®1.0 was used toprogram and run the experiments. All participantsunderstood the instructions that were impartedand went through the experimental protocol in thefollowing order: the time discrimination task, theStroop task, and the n-back task, with each taskbeing preceded by a practice phase.

Time discrimination task

A time discrimination task (reminder method) wasutilized. Each trial was composed of a standard

and a comparison stimulus presented sequentiallyin a fixed order (standard-comparison). The stimuliused were black-and-white smiley faces, presentedat the centre of a grey background. Two stan-dard durations were employed: 500 and 1,300 ms.The comparison stimulus was ±25% longer orshorter than the standard duration: standard–long(500/625 ms and 1,300/1,625 ms) or standard–short (500/375 ms and 1,300/975 ms).

Each trial was presented 12 times in a ran-dom order. Participants were instructed to pressone of two keys marked as L or B: L if the sec-ond time interval was longer than the first (“L”refers to the Italian word “lungo” = long), B ifthe second time interval was shorter than the first(“B” refers to the Italian word “breve” = short).Participants were instructed to respond with theirindex fingers, and the response keys were balancedbetween subjects. A practice phase was included atthe beginning of the task to ensure that instructionswere clear. Participants performed each pair ofstimuli (500/625 ms; 500/375 ms; 1,300/1,625 ms;

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1,300/975 ms) one time, the stimuli were the sameas those used in the task. No feedback on perfor-mance was provided.

Attention, working memory, andspeed-of-processing tasks

A Stroop task was employed to study the attentionand speed-of-processing components. Each trialwas composed of three colored words displayed atthe centre of the computer screen for 2 s. The wordsat the centre (variably RED, YELLOW, GREEN,and BLUE) were presented in 20-point-size Arialfont and were colored in red, yellow, green, orblue, while the words to the right and left werealways in black. The central word was the targetstimulus, whereas the two black lateral words werethe possible responses (i.e., GREEN RED RED).Participants were instructed to judge the color ofthe central word by pressing a key on the keyboardmarked with an arrow pointing either right (→) orleft (←), depending on the position of the correctresponse. Whenever the answer was on the left, the(←) key had to be pressed with the left index finger,and whenever the answer was on the right, the (→)key had to be pressed with the right index finger.Two possible conditions were randomly presented:congruent and incongruent. In the congruent con-dition, the color of the central word correspondedto the written word (the word “RED” written withred ink). In the incongruent condition, the colordid not match the written word (the word “RED”written with green ink). Forty-eight stimuli werepresented in each condition (for a total of 96 stim-uli), and an equal number of correct responseswere presented on the right or left of the centralword (see Del Missier, Mäntylä, & Bruine de Bruin,2010). A practice phase was included at the begin-ning of the task to clarify the instructions and tofamiliarize with the task: Participants performed10 trials, 5 in the congruent and 5 in the incongruentcondition.

The n-back task was employed to study the work-ing memory component (for a review see Owen,McMillan, Laird, & Bullmore, 2005). The stim-uli were common two-syllable words presented atthe centre of the computer screen and written in36-point size Courier New font in white ink on ablack background. Participants were instructed toindicate, by pressing the left mouse key, when theword that appeared was the same as the one pre-sented 2 words back. The task comprised 48 targetstimuli (24 different stimuli presented 2 times) and48 nontarget stimuli; 12 nontarget stimuli were pre-sented only once, 12 stimuli were 3-back, 12 stimuli

were 4-back, and 12 stimuli were 5-back. A practicephase was made at the beginning of the task to clar-ify the instructions and to familiarize with the task.Five target words and 10 nontarget words were pre-sented during the practice phase; no feedback onperformance was provided.

RESULTS

Time discrimination task

The time discrimination task was analyzed interms of response accuracy reflecting the percent-age of correct responses. Data were analyzed viaa mixed-model analysis of variance (ANOVA) withgroup (TBI vs. control) as a between-group factor,and within factors of standard duration (500 vs.1,300 ms) and comparison duration (short vs. long).The significance level for this and all the subsequentanalyses was p < .05. The post hoc analyses wereperformed with the Bonferroni correction.

The main effect of group, F(1, 52) = 27.60,MSE = 0.957, p < .001, η2

p = .347, and standardduration, F(1, 52) = 6.34, MSE = 0.125, p < .05,η2

p = .109, were significant, whereas the main effectof the comparison duration did not reach the signif-icance level, F(1, 52)= 0.22, MSE = 0.011, p= .64,η2

p = .004. The TBI patients were less accurate thanthe controls (70% vs. 83%). The participants weremore accurate when discriminating the 1,300-msduration than when discriminating the 500-msduration (79% vs. 74%). The Group × StandardDuration, F(1, 52) = 4.34, MSE = 0.086, p < .05,η2

p = .077, and Standard Duration × ComparisonDuration, F(1, 52) = 79.02, MSE = 1.938, p <

.001, η2p = .603, interactions were significant.

These interactions were qualified by the signifi-cant Group × Standard Duration × ComparisonDuration interaction, F(1, 52) = 14.22, MSE =.349, p < .0001, η2

p = .215 (Figure 1a). Post hocanalyses indicated significant differences betweengroups when the standard interval was 500 ms, andthe comparison condition was long (500–625 ms).The pattern was reversed when the standard inter-val was 1,300 ms. In fact, TBI patients were signifi-cantly less accurate in the short comparison condi-tion (1,300–975 ms). No significant differences werefound between groups in the short condition whenthe standard interval was 500 ms (p = .241) or inthe long condition when the standard interval was1,300 ms (p = .201).

We analyzed how many times the key waspressed to investigate how the relative durationof the two stimuli affects temporal performance.Data were analyzed via a mixed-model ANOVA

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A

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Figure 1. (A) Accuracy in the time discrimination task as afunction of standard duration, comparison duration, and group.(B) Number of key presses as a function of standard duration,comparison duration, and group. In both figures, error bars arepresented, and “short” and “long” refer to the duration (−25%or + 25%) of the comparison stimulus. TBI = traumatic braininjury.

with between-groups factor group (TBI vs. control)and within factors of standard duration (500 vs.1,300 ms) and comparison duration (short vs. long).No main effect of group, F(1, 52) = 1.72, MSE =0.167, p = .195, η2

p = .032, stimulus duration,F(1, 52)= 2.00, MSE = 0.019, p= .163, η2

p = .037,or comparison duration, F(1, 52) = 1.07, MSE =31.13, p = .304, η2

p = .020, were found. Thesignificant interactions of Standard Duration ×Comparison Duration, F(1, 52) = 121.50, MSE =10.48, p < .001, η2

p = .556, and Group × StandardDuration×Comparison Duration, F(1, 52)= 7.53,MSE = 121.50, p < .001, η2

p = .127 (Figure 1b)are considered a particularly interesting finding.Post hoc analysis showed that both groups had asignificantly greater tendency to respond “short”when the standard duration was 500 ms and “long”when the standard duration was 1,300 ms. Withregard to the 500-ms standard stimulus, a signif-icant difference was found between groups in the

long condition. TBI patients considered the com-parison stimulus shorter than the standard one evenin the long condition. When the standard stimuluswas 1,300 ms, no significant differences were foundbetween groups.

Attention, speed-of-processing, and workingmemory tasks

Three separate independent t test analyses were per-formed. We analyzed the Stroop data in terms ofreaction time (RT) and defined the attention indexas the difference between incongruent and congru-ent RT. The results revealed significant differencesbetween groups, t(45) = 2.73, p < .01, d = 1.27.TBI were more affected by interference than werecontrols (261 vs. 141 ms). The speed-of-processingindex was obtained by analyzing the RT in the con-gruent condition of the Stroop task.1 Significantdifferences were found between the TBI patientsand the controls, t(46) = 5.57, p < .001, d = 1.56,indicating that the former were slower in elaborat-ing and responding to simple information (1,272 vs.970 ms). N-back data were analyzed in termsof number of errors (false alarms + omissions),and a significant difference was found between thegroups, t(52) = 1.97, p < .01, d = 0.53, indicatingthat the TBI patients produced more errors than thecontrols (9.51 vs. 7.07). Performance on n-back taskwas used to measure the working memory index.

Correlations between time perception,attention, speed of processing, and workingmemory

To examine the relationship between time percep-tion, attention, speed-of-processing, and workingmemory abilities, two separate two-tailed Pearsoncorrelation analyses were performed for TBIpatients and controls (see Table 3). Four sepa-rate indices were calculated for the time discrim-ination task, and each represented the mean ofthe participants’ accuracy in the four conditions(500–short, 500–long, 1,300–short, and 1,300–long). The attention index (attention), the speed-of-processing index (speed of processing), and theworking memory index (working memory) werealso computed.

Significant correlations were found in the TBIcohort, when the standard duration was 500 ms,

1We thank an anonymous reviewer for suggesting this measureas index of speed of processing.

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TABLE 3Pearson’s correlations between time discrimination, attention, working memory, and speed-of-processing indices separately for

TBI patients and controls

TBI patients Control group

Standard 500 ms Standard 1,300 ms Standard 500 ms Standard 1,300 ms

Index Short Long Short Long Short Long Short Long

Attention −.113 −.163 −.472∗ −.242 −.201 −.209 −.024 −.578∗∗Working memory −.394∗ −.226 −.331∗ −.567∗∗ .005 .211 −.350∗ −.332∗Speed of processing −.386∗ −.121 −.376∗ −.336∗ −.313 −.147 −.348∗ −.361∗

Note. TBI= traumatic brain injury. “Short” referred to the –25% duration of the comparison stimulus, and “long” referred to the+25%duration of the comparison stimulus. Attention = difference between the reaction times (RTs) in incongruent and congruent trials inthe Stroop task. Working memory = number of errors in the n-back task. Speed of processing = RT in the congruent condition of theStroop task. The analysis has been conducted separately on TBI patients and controls.∗p < .05. ∗∗p < .01.

and the comparison was short, with working mem-ory and speed-of-processing indices. It was foundthat TBI patients with better working memory andspeed-of-processing abilities were also more accu-rate at discriminating between the two intervals.No other significant correlations were found withregard to the 500-ms standard duration (with eitherthe short or long comparison duration) and atten-tion, working memory, and speed of processing inthe TBI or controls.

Interestingly, significant correlations were foundbetween time discrimination, when the standardduration was 1,300 ms, and the comparison dura-tion was short or long, with working memory andspeed of processing in both TBI patients and con-trols. Attention was involved differently in the twogroups. Taken together, the results indicate that par-ticipants with better cognitive resources have bettertemporal abilities and that cognitive involvementis differentiated depending on the standard andcomparison durations utilized.

Correlations between number of key presses,attention, working memory, and speed ofprocessing

Two separate two-tailed Pearson correlation anal-yses were performed for TBI patients and con-trols. Four separate indices were calculated forthe time discrimination task: Each represented thenumber of key presses for the four conditions(500–short, 500–long, 1,300–short, and 1,300–long). The attention index, the speed-of-processingindex, and the working memory index were alsocomputed.

The only significant correlation was found incontrol patients when the standard duration was500 ms, and the comparison duration was shorter,

with the index of speed of processing, r(52)= –.357,p < .05. Attention and working memory indiceswere not correlated with the number of key presses.

DISCUSSION

How different brain regions encode and elabo-rate temporal information and what cognitive pro-cesses are involved in time perception are intriguingsubjects. In the present study, TBI patients andhealthy controls were asked to undertake a dis-crimination task. Involvement of attention, work-ing memory, and processing speed in discriminat-ing time intervals shorter or longer than 1 sec-ond was also evaluated. Previous studies on TBIpatients have described higher variability (Mioniet al., 2012; Perbal et al., 2003) and less accuracywhen TBI patients were tested with time inter-vals exceeding the working memory span (above30 s; Anderson & Schmitter-Edgecombe, 2011;Schmitter-Edgecombe & Rueda, 2008). The liter-ature on time perception in frontal lobe patientshas, however, outlined temporal dysfunction evenwhen those patients are tested using shorter inter-vals in the milliseconds range (Casini & Ivry, 1999;Harrington et al., 1998; Mangels et al., 1998;Nichelli et al., 1995; Picton et al., 2006; Rubia &Smith, 2004).

The innovative aspect of the present work wasusing a time discrimination task to investigatethe temporal ability of TBI patients and to testdurations longer and shorter than 1 second. Ourresults showed temporal dysfunction in TBI. In par-ticular, TBI patients were found to be significantlyless accurate when discriminating 500 ms than whendiscriminating 1,300 ms, while no significant differ-ences were found between durations in the controlgroup. Discriminating 500-ms durations seems to

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be extremely challenging for TBI patients, whencompared to controls, presumably because of theadditional cognitive functions involved in time dis-crimination tasks.

The results concerning the number of keyspressed can be considered a particularly interest-ing outcome of this study. While previous stud-ies on time perception had already described thepresence of a time-order error (the interactionbetween standard duration and comparison dura-tion; Hellström, 1985; Hellström & Rammsayer,2004; Wiener, Turkeltaub, & Coslett, 2010), it hasoften been neglected and has never been investi-gated in TBI patients. Comprehending the interac-tion between standard and comparison durations,via the number of times the keys were pressed,also adds further depth to the study, providingadditional information on the cognitive processesinvolved in time discrimination in TBI patients.

If only accuracy had been taken into consid-eration, the conclusion would have been, on thebasis of those data, that TBI patients present tem-poral impairment only when the 500-ms standardduration was followed by the longer comparisonduration and when the 1,300-ms standard durationwas followed by the shorter comparison duration.However, the similar performance noted in TBIpatients and controls, when the 500-ms standardduration was followed by the shorter comparisonduration and when the 1,300-ms standard durationwas followed by the longer comparison duration,may have been obscured by a response bias (numberof keys pressed). Bearing in mind that the cor-rect number of times the keys should have beenpressed for each condition (500–long, 500–short,1,300–long, and 1,300–short) was 12, analyzing thenumber of times keys were really pressed shoulduncover the response bias. When the 500-ms stan-dard duration was presented, patients with TBIpressed the “short” key significantly more timesthan the controls did, whereas when the 1,300-msstandard duration was presented, patients with TBIpressed the “long” key significantly more times.It should be pointed out that both groups had agreater tendency to respond “short” when the stan-dard duration was 500 ms and “long” when thestandard duration was 1,300 ms, but this tendency(response bias) was greater in TBI patients when500-ms duration was presented.

The number of times the keys were pressed didnot correlate with attention or working memoryindices for either the TBI patients or the con-trols, confirming that this aspect was not cognitivelycontrolled but is more likely to be subcortically con-trolled and represent a response bias. Our findingsare consistent with previous studies that indicate a

significant interaction between standard and com-parison durations in healthy adults (Gontier et al.,2007; Gontier et al., 2009; Le Dantec et al., 2007;Paul et al., 2003), and now data concerning TBIpatients showing a greater response bias can beadded to the literature.

Various explanations may account for the pat-tern described. One could be linked to a memoryinterference in which the representation of any stim-ulus in memory decays after a certain time limit(Baddeley, 1992). Memory interference may havemade the first stimulus appear shorter than thesecond one especially with reference to the 1,300-ms standard duration when the long comparisoncondition was characterized by better performance.It is possible that the standard stimulus appearedshorter due to memory interference, and the dif-ference between the standard and the comparisonseemed more detectable (Paul et al., 2003). But thiswas not the case for the 500-ms standard dura-tion, in which case the better performances werenoted in the reverse condition (in the short compar-ison condition). For durations shorter than 1 s, atthe limit of the memory span, the “short” responsemay be activated automatically (Le Dantec et al.,2007; Paul et al., 2003). Lewis and Miall (2003b)reported that shorter intervals are generally pro-cessed in a less controlled manner than longer ones,with the former relying more on subcortical regions(Mangels et al., 1998).

A wider interpretation that takes into accountshort and long durations was provided by Gontieret al. (2007), who suggested that participants createan “anchor” stimulus in their memory and clas-sify stimuli approximately as below the “anchor”when short and above the “anchor” when long(see also Oshio, Chiba, & Inase, 2006). This couldalso be the case in our study: The participantscreated a memory representation of “anchor” dura-tion by averaging out the shorter (375 ms) and thelonger (1,625 ms) durations presented and classi-fied stimuli in relation to the “anchor.” Workingmemory is required to create and maintain the rep-resentation of the “anchor” duration active, anda working memory dysfunction may have alteredthe representation of the “anchor” duration andsubsequently affected temporal performance in TBIpatients.

Previous studies showed that different systemsare involved in perceiving duration in the millisec-onds and seconds rage (Lewis & Miall, 2003a,2003b; Mangels et al., 1998; Nichelli, Always, &Grafman, 1996; Nichelli et al., 1995; Rubia, 2006;Rubia & Smith, 2004). Our results seem to supportprevious studies confirming that a more cognitivelycontrolled system is involved when longer durations

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(longer than 1 second) are being assessed (Buhusi& Meck, 2005; Handy, Gazzaniga, & Ivry, 2003;Lewis & Miall, 2003a, 2003b). In fact, there weresignificant correlations in both groups, when thestandard duration was 1,300 ms, with attention,working memory and speed-of-processing indices.Participants with better cognitive abilities shouldalso present better temporal abilities (Block &Zakay, 2006). During time discrimination tasks,working memory resources seem to be involvedwhen participants are required to bear in mind arepresentation of the standard intervals to make thesubsequent decision, but a disruption in attentionhas also been shown to affect temporal perception(Casini, Macar, & Grondin, 1992; Grondin, 2010;Grondin & Macar, 1992; Mangels et al., 1998).Finally, at the decision stage, adequate speed-of-processing abilities are required to accurately per-ceive the two intervals and to judge their relativeduration. The fact that there were no significantcorrelations between the 500-ms standard dura-tion and attention, working memory, or speed-of-processing indices in the controls seems to supportthe hypothesis that temporal intervals shorter than1 s are processed in a more automatic mannerand require less involvement of high cognitive pro-cesses (Lewis & Miall, 2003a, 2003b). Interestingly,significant correlations were found only in TBIpatients, when the standard duration was 500 ms,and the comparison duration was short, with work-ing memory and speed-of-processing indices. TBIpatients seem to require additional cognitive abili-ties to discriminate temporal intervals shorter than1 second.

Neuroimaging (Gontier et al., 2007; Ivry &Spencer, 2004; Lewis & Miall, 2003b; Macar et al.,2002; Paul et al., 2003; Smith, Taylor, Lidzba, &Rubia, 2003) and patient studies (Ivry & Spencer,2004; Mangels et al., 1998; Nichelli et al., 1996;Nichelli et al., 1995) have identified different brainregions involved in the time perception networkconfirming the distinction between automatic andcognitively controlled temporal systems (Rubia,2006; Rubia & Smith 2004). Some have hypoth-esized that the cerebellum is the locus of theinternal clock, which is involved when milliseconddurations are being considered (Ivry & Spencer,2004; Rubia, 2006). The prefrontal cortex, thoughtto be the locus of counting mechanisms and storageand retrieval of temporal information, is involvedin perceiving longer temporal intervals (Mangelset al., 1998; Nichelli et al., 1995; Rubia, 2006).

Mangels et al. (1998) showed temporal impair-ment in neocerebellar patients in both milliseconds

(400 ms) and seconds (4 s) ranges, whereas frontalpatients presented temporal impairment only inrelation to longer durations, mainly due to work-ing memory dysfunction. Nichelli et al. (1995),instead, showed temporal impairment in frontalpatients with reference to both short (100–900 ms)and long time intervals (8–32 s). In accordancewith Nichelli et al.’s findings, our data demon-strated that TBI patients present temporal dysfunc-tion even when tested with intervals falling in themilliseconds range. The nature of the group dif-ferences on this task indicates a disruption at thedecisional level, with TBI patients utilizing a dif-ferent processing system when they are forced tomake rapid decisions. Attention, working mem-ory, and speed of processing were involved intime perception particularly when participants wererequired to discriminate durations longer than asecond, but TBI patients also required workingmemory and speed-of-processing abilities to dis-criminate intervals shorter than a second. The dif-ferent pattern noted in the involvement of atten-tion, working memory, and speed of processingin TBI patients and controls gives additional sup-port to the hypothesis that there are two differentsystems that govern the perception of intervalsshorter or longer than 1 s (Lewis & Miall, 2003a,2003b).

Future studies could recruit TBI patients accord-ing to the type of lesion (frontal or nonfrontal)to further investigate how the type of lesion isinvolved or differently affects temporal judgments.Although attention, working memory, and speed-of-processing deficits are well documented in TBIpatients (Knight et al., 2005), and the involvementof high cognitive abilities in time perception hasbeen described in the literature (Perbal et al., 2003;Zakay & Block, 2004), only a limited number ofstudies have attempted to investigate time percep-tion in TBI. As impaired time perception couldaffect the daily adaptive functioning of patientsrecovering from TBI (Fleming et al., 2008), thisstudy could have important clinical implicationsfor time perception rehabilitation, which shouldfocus not only on improving temporal abilities butalso on attention, working memory, and speed-of-processing components. Specific tasks utilizingboth time intervals (shorter or longer than 1 s)need, in fact, to be designed and developed to helprehabilitation projects.

Original manuscript received 22 March 2012Revised manuscript accepted 29 November 2012

First published online 24 December 2012

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