http://informahealthcare.com/bij ISSN: 0269-9052 (print), 1362-301X (electronic) Brain Inj, 2015; 29(3): 343–351 ! 2014 Informa UK Ltd. DOI: 10.3109/02699052.2014.976273

ORIGINAL ARTICLE

Impaired practice effects following mild traumatic brain injury: An event-related potential investigation Jeffrey M. Rogers1, Allison M. Fox2, & James Donnelly3 School of Psychology, Australian Catholic University, Strathfield, NSW, Australia, 2School of Psychology, University of Western Australia, Crawley, WA, Australia, and 3School of Health & Human Sciences/Psychology, Southern Cross University, Coffs Harbour, NSW, Australia

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Abstract

Keywords

Background: The negative effects of mild traumatic brain injury (mTBI) on attention are well established. Effects of practice on neuropsychological test performance have also been long recognized and more recently linked to electrophysiological indices of information processing. Objective: The current study examined the behavioural and electrophysiological impact of mTBI on consistent practice of a neuropsychological test of attention. Research design: Prospective cohort study. Methods: Adult participants with a history of mild TBI (n ¼ 10; time since injury 4 2 months, mean ¼ 15.2 months) and healthy matched controls (n ¼ 10) completed the Paced Auditory Serial Addition Task (PASAT) at four separate sessions. Event-related potentials (ERPs) were simultaneously recorded. Results: Accuracy of PASAT performance in both groups improved significantly with practice. In healthy controls behavioural improvements were associated with significant attenuation of a frontally distributed ERP component marker of executive attention. These executive attention demands did not appear to ease with consistent practice in the mTBI group, who also endorsed more concussion-related symptoms. Conclusions: These preliminary results suggest sustained mental effort is required to achieve ‘normal’ performance levels following mTBI and support the use of practice-related, ERP indices of recovery from mTBI as a sensitive correlate of persistent post-concussion symptoms.

Attention, event-related potentials, mild TBI, PASAT, practice effects

Background Mild traumatic brain injury (mTBI) can disrupt a range of cognitive functions, most apparent in the domains of attention and information processing [1–3]. After mTBI, individuals frequently report slowed thinking, poor concentration, distractibility and difficulty attending to more than one task at a time [4, 5]. However, the concept of attention encompasses a broad range of cognitive abilities and attempts to identify specific impairments following mTBI have produced inconsistent results. Some of the most consistent findings have come from studies investigating the integrity of executive attentional processes, variously referred to as controlled processing [6], the central executive [7] or supervisory attentional control [8]. Performance on simple reaction time and vigilance tasks following mTBI typically remains intact, presumably because these proceed relatively automatically. In contrast, complex choice reaction time tasks have regularly revealed performance deficits [9, 10] and a decreased capability for strategic control over attentional

History Received 21 January 2014 Revised 20 August 2014 Accepted 8 October 2014 Published online 28 November 2014

resources required for the co-ordination and execution of novel task requirements has been argued to lie at the core of the attention deficit in mTBI [10–12]. The dual-process model of information processing [6] contends that executive attentional control is not a solitary concept, but rather represents the extreme of a continuum. At one end, executive attention processes modulate the acquisition of new and complex information under the individual’s direct and active control. At the other end, following regular practice in a consistent environment, the effortful, serial activity directed by executive attention is gradually replaced with an effortless, parallel retrieval mechanism as associations within and between information processing networks are strengthened through repeated activation. Executive attention is, therefore, involved in the strategies and behaviours generated on the first attempts to process complex or novel information and only ceases when a set of well learned processes and automatic triggers appropriate to the situation have been established [13]. The Paced Auditory Serial Addition Test

Correspondence: J. Rogers, School of Psychology, Australian Catholic University, Locked Bag 2002, Strathfield, NSW, 2135, Australia. Tel: +61 2 9701 4538. Fax: +61 2 9746 3059. E-mail: [email protected]

The Paced Auditory Serial Addition Test (PASAT [14]) is a well-established measure of attentional functioning following head injury [15, 16], with demonstrated sensitivity

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to mTBI [12, 17–19]. The PASAT involves continuous auditory presentation of a random sequence of 61 digits from 1 through 9. Examinees are required to calculate the sum of the most recently presented digit and the digit presented immediately prior, while simultaneously attending to the next digit in the series. Thus, the second digit is added to the first, the third to the second and so on. Each trial requires the examinee to register sensory input, retrieve a stored stimulus, perform a mental calculation, respond verbally and inhibit encoding of their response while attending to the next stimulus in the series, all at an externally determined pace [20]. Successful PASAT performance, therefore, relies upon the efficient co-ordination of the various sub-tasks into one single integrated activity [21, 22] and the sensitivity of the PASAT to mTBI stems from these demands upon executive attention [4, 12, 15]. Of note, significant practice effects have been observed in healthy controls repeatedly administered the PASAT [23–25]. The improvement in performance over successive administrations of the PASAT has been hypothesized to be due to an active learning process directing the strategic processing of target stimuli and suppression of distracting stimuli [24, 26]. Event-related potentials Functional techniques such as event-related potentials (ERPs) can provide information on the timing and integrity of neural processes that mediate a given cognitive operation. ERPs possess the high temporal resolution necessary to identify at which particular stage of information processing any abnormality is occurring and can also provide an index of the intensity of activation in the underlying neural generators. Studies of the brain mechanisms of attention have extensively and successfully utilized ERPs as fast-scale indices of information processing [27] and have consistently identified electrophysiological markers of attentional aspects. In particular, the late Processing Negativity (PN) component of the ERP waveform is believed to reflect voluntary, limitedcapacity activity within frontally distributed higher order attention and working memory components, responsible for co-ordinating and maintaining goal-directed processing of stimuli [28–31]. Examination of late PN component amplitude has previously discriminated healthy control subjects from individuals with mTBI, although, somewhat paradoxically, injury has been associated with both amplitude augmentation [32] and attenuation [28, 30]. Reductions in late PN component amplitude have been linked to impairments in the allocation of executive attentional resources and are generally consistent with findings from the P300 literature of a decline in information processing capacity following mTBI [28, 30]. In contrast, amplitude augmentation has been interpreted as evidence of a compensatory strategy, wherein normal behavioural performance is achieved through an abnormally enhanced allocation of executive attention resources [32]. Finally, research devoted to exploring the effects of practice on the late PN component has provided a robust effect. Over repeated testing sessions of an auditory oddball task a practice-mediated reduction in late PN amplitude has been reported [31, 33, 34]. In each study, amplitude

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attenuation was accompanied by increases in task accuracy. More recently, administration of the PASAT over four sessions in healthy participants was associated with significant improvements in task accuracy and a significantly reduced late PN component amplitude, as practice seemingly eased strategic planning and co-ordination requirements the task places on frontally-mediated executive attention resources [25]. Aims of the current study The capacity for strategic control over attentional resources required for the co-ordination and execution of complex task requirements appears to be disrupted following mTBI [10– 12]. According to the dual process model [6], this may not only impair novice PASAT performance, but also disrupt practice-dependent plasticity mechanisms underlying development of automatic task processing. However, this has not been explored, as the PASAT provides no direct measure of information processing intensity, or the effects of practice on specific aspects of brain function. The purpose of this experiment was to, therefore, combine behavioural and electrophysiological measures of PASAT performance to provide a unique description of the effects of mTBI on executive attention processes during novel and practiced performance. Over an extended training period participants with mTBI were expected to demonstrate less benefits of practice on the PASAT. This was predicted to appear as abnormally elevated and sustained amplitude of the late PN component over time and less improvement in behavioural performance, relative to healthy controls.

Methods Participants This research was approved by the Human Research Ethics Committee of the University of Western Australia and each participant provided written informed consent for voluntary participation. Ten individuals with a single, self-reported mTBI and 10 healthy individuals matched for age, gender and education were recruited from a university community. All participants had normal hearing and normal or corrected to normal vision and no self-reported history of psychiatric or neurological disorder or drug abuse. Additional participant characteristics are presented in Table I. mTBI diagnosis was established during a semi-structured screening process with the study neuropsychologist (JR) using criteria defined by Kay et al. [35]: injuries resulting in an alteration in mental state associated with loss of consciousness not exceeding 30 minutes and a period of post-traumatic amnesia no longer than 24 hours. Injury characteristics were categorized using commonly applied classification systems [36] and are summarized in Table II. Task Participants were administered the computerized, children’s version of the PASAT [14]. The children’s version of the task presents numbers from 1 through 9, but minimizes the possible confounding effect of mathematical ability on performance by restricting sums to 10 or less [37]. A trial

mTBI practice effects

DOI: 10.3109/02699052.2014.976273

Table I. Characteristics of the mTBI and control groups. Significance levels of group differences are indicated in the last column. mTBI group

Control group

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N (Gender) 10 (4 F, 6 M) 10 (4 F, 6 M) Handedness 10 R 9 R, 1L Age (years) at Injury Mean (SD) 20.2 (4.1) NA Range (Median) 16–29 (18) Time (months) since injury Mean (SD) 15.2 (18.1) NA Range (Median) 2–60 (9) Age (years) at testing Mean (SD) 21.1 (5.6) 21.0 (4.5) Range (Median) 17–34 (18) 18–30 (18.5) Years of Education Mean (SD) 14.2 (2.3) 13.9 (2.4) Range (Median) 13–20 (13) 11–20 (13)

Significance

p ¼ 1.0 p ¼ 0.8

Table II. Injury characteristics of the mTBI group. Time since Age at injury injury (years) Gender (months) 16 17 16 18 20 29 18 17 22 24

M M M M M M F F F F

2 2 16 4 10 60 6 8 12 32

Nature of Iinjury

Time unconscious

Length of PTA

recreation recreation recreation recreation recreation fall MVA fall recreation recreation

51 minute 51 minute 1–5 minutes 51 minute 51 minute 51 minute 51 minute 10–15 minutes 1–5 minutes 1–5 minutes

51 hour 1–24 hours 51 hour 51 hour none none 1–24 hours 1–24 hours none 1–24 hours

MVA, passenger in a motor vehicle accident.

consisted of 61 digits (60 sums) and testing sessions included trials at each of four inter-stimulus interval (ISI) rates (2.4, 2.0, 1.6 and 1.2 seconds). Digits were presented via headphones and spoken responses were registered via a microphone and digital recorder for offline analysis.

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cognitive or behavioural activity which is only marginally or not at all different from any deficits elicited post-injury. To address this, participants were administered the Wechsler Test of Adult Reading (WTAR) [38] to provide an estimate of their pre-morbid level of intellectual functioning. Non-organic factors including insufficient motivation [39] and incentive for secondary gain [40] have been implicated in the case of persisting cognitive and behavioural complaints following mTBI. Individuals involved in litigation were excluded from the current study and the Rey 15 Item Memory Test [41] was administered to provide a brief screen of each participant’s level of effort and propensity to exaggerate complaints. PASAT performance is related to mathematical ability and the PASAT should not be interpreted as a measure of attentional processes when mathematical skills are poor [19]. The Numerical Operations sub-test of the Wechsler Individual Achievement Test-Second Edition (WIAT-II) [42] was, therefore, administered to assess mathematical ability. Examinees may react with aversion to the PASAT [43, 44] and concerns that subjective mood state can negatively affect performance independent of attentional functioning have been raised [44]. Furthermore, mood disturbance has been implicated in the generation and maintenance of cognitive and behavioural symptomatology following mTBI [18]. The Depression Anxiety Stress Scale (DASS) [45] was, therefore, administered to provide a clinical rating of each participant’s current self-reported levels of depression, anxiety and stress. To evaluate the nature and severity of self-reported postinjury cognitive and behavioural symptomatology, participants completed the Post-concussion Syndrome Checklist (PCSC) [46]. The PCSC was chosen over other available checklists [47, 48], as they do not include measures of symptom frequency to distinguish between respondents experiencing only rare symptoms and those with a high rate of symptoms. In addition, these checklists do not request information on the duration or severity of symptoms, which can vary considerably from one respondent to another [46]. EEG acquisition and analysis

Procedure Participants attended four sessions over a mean 10.95 day period (SD ¼ 4.51 days, range ¼ 4–17 days). The two experimental groups did not differ in length of time of the testing interval [t(18) ¼ 1.04, p ¼ 0.31]. To maximize the amount of data available for analysis, during each experimental session participants were administered two PASAT blocks (A and B), with a short break in between. Each block consisted of a randomized order of presentation of PASAT trials at the 2.4, 2.0, 1.6 and 1.2 second ISI rates. Total number of correct responses on each trial (max ¼ 60) was averaged across blocks and selected for analysis of performance accuracy. Participants were asked to minimize eye and body movements and speak quietly when responding. During PASAT administration continuous electroencephalogram (EEG) activity was simultaneously recorded (see below). To begin experimental Session 1, a series of instruments were administered to all participants. First, a concern in outcome studies is the possibility of a pre-morbid history of

Continuous EEG recordings were obtained using a Neuroscan QuikCap with 32 tin electrodes placed according to the International 10–20 system. Vertical and horizontal electro-oculograms were recorded from electrodes placed at the supraorbital ridge and suborbital region of the left eye and outer canthus of each eye. All electrodes were referenced to nose electrodes and impedances adjusted to below 6 kV. EEG activity was sampled continuously at a digitization rate of 250 Hz. Signals were amplified with a Neuroscan Inc. (Herndon, VA) SynAmps system with a band-pass filter of 0.05–30 Hz (6 dB down). SCAN 4.0 software registered and analysed EEG activity. Prior to averaging, statistical eye movement correction was performed offline using the principal components transform included in the SCAN software. After baseline adjustment around a 100 millisecond pre-stimulus interval, remaining epochs containing amplitudes in excess of ± 75 mV at any electrode were rejected. PASAT stimulus-locked cognitive ERPs were then averaged over 1-second epochs, including a

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Table III. Mean neuropsychological test scores (standard deviations). Significance levels of group differences are indicated in the last column.

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WTAR Predicted FSIQ WIAT-II Numerical Operations Score DASS Depression Score DASS Anxiety Score DASS Stress Score

mTBI group

Control group

Significance

108.7 (4.8) 108.6 (9.5)

110.9 (4.1) 109.1 (9.0)

p ¼ 0.3 p ¼ 0.9

5.7 (7.0) 4.6 (5.1) 9.6 (7.1)

2.3 (2.2) 2.4 (2.6) 7.0 (6.6)

p ¼ 0.2 p ¼ 0.2 p ¼ 0.4

Table IV. Mean correct PASAT responses (standard deviations). Higher scores reflect better performance (max ¼ 60). Inter-stimulus interval

100 millisecond pre-stimulus baseline period and a 900 millisecond post-stimulus period. Criteria derived from visual inspection of control group grand-averaged Session 1 waveforms were used to determine the electrode site over which the late PN component reached maximum activation. Mean amplitude (mV) and peak latency (ms) was then calculated from this site. As such, late PN was defined as the mean negativity in the interval 380–650 milliseconds, measured from the fronto-central electrode Fz.

2.4 s

2.0 s

1.6 s

1.2 s

mTBI group Session 1A Session 1B Session 2 Session 3 Session 4

52.2 53.3 57.0 56.1 57.3

(5.1) (7.0) (2.2) (4.0) (2.6)

49.6 53.1 54.9 56.1 56.0

(7.4) (6.1) (4.6) (5.0) (5.0)

46.4 49.6 52.7 54.2 56.0

(9.7) (7.2) (5.5) (5.7) (6.0)

39.4 43.0 47.9 51.6 54.3

(9.1) (11.0) (9.3) (8.3) (7.9)

Control group Session 1A Session 1B Session 2 Session 3 Session 4

48.1 50.9 54.2 56.2 57.2

(5.0) (5.6) (4.2) (2.5) (2.3)

42.7 47.4 51.9 53.3 55.3

(9.0) (6.9) (5.1) (3.6) (2.8)

38.7 41.7 49.1 50.8 51.9

(9.3) (8.03) (7.9) (4.2) (5.6)

32.6 34.7 42.0 48.1 49.5

(6.4) (7.3) (8.1) (6.6) (7.5)

Independent samples t-tests revealed no difference between the mTBI and control groups in WIAT-II mathematical ability [t(18) ¼ 0.12, p ¼ 0.91] or WTAR estimated full scale IQ [t(18) ¼ 1.10, p ¼ 0.29] (see Table II), with both groups functioning in the Average to High Average range [38, 42]. All participants performed without error on the Rey 15-Item Test. Current DASS levels of depression [t(18) ¼ 1.48, p ¼ 0.16], anxiety [t(18) ¼ 1.22, p ¼ 0.24] and stress [t(18) ¼ 0.85, p ¼ 0.41] were equivalent between the two groups and within the normal range [45]. On the PCSC, mTBI participants reported suffering from more intense [t(18) ¼ 2.31, p ¼ 0.03] and prolonged [t(18) ¼ 2.28, p ¼ 0.04] headache symptoms than healthy controls and experiencing difficulty concentrating, which was more severe [t(18) ¼ 2.45, p ¼ 0.03] and longer lasting [t(18) ¼ 2.29, p ¼ 0.03].

combining behavioural data across these two blocks as planned, ISI data from each Session 1 block (A and B) were, therefore, analysed separately. Repeated measures ANOVA identified no further significant differences and the remaining sessions were averaged into single blocks for analysis. Participants in both experimental groups demonstrated improvement in the mean number of correct PASAT responses over the four experimental sessions and with increasing ISI. Although participants with mTBI tended to provide more correct responses than the control group (see Table IV), the main effect of group was not significant [F(1,18) ¼ 2.83, p ¼ 0.11, p2 ¼ 0.14]. For the mean number of correct PASAT responses, the main effects of session [F(2.02, 36.43) ¼ 91.16, p50.01, p2 ¼ 0.84] and ISI [F(1.35, 24.24) ¼ 51.85, p50.01, p2 ¼ 0.74] were significant. The interaction between ISI and session was also significant [F(4.98, 89.57) ¼ 10.51, p50.01, p2 ¼ 0.37]. In addition to the previously noted improvements from Session 1A to 1B, Bonferroni corrected (p50.0125) paired-samples t-tests indicated the mean number of correct PASAT responses also significantly improved from Session 1B to Session 2 at every ISI in both groups.

Behavioural results

ERP results

To investigate the effects of practice, two-way repeated measures ANOVAs with ISI (2.4, 2.0, 1.6, and 1.2 seconds) and session (1A, 1B, 2, 3, 4) as within-subjects factors and group (mTBI and control) as a between-subjects factor were conducted to compare the mean number of PASAT correct responses at each experimental session and ISI. Where Mauchly’s test of sphericity was violated, GreenhouseGeisser corrections were applied. During testing, inconsistencies with the PASAT response recording software resulted in losses of behavioural data from Session 1A of one control participant and Session 3B of another control participant. PASAT behavioural results for these participants were imputed with the group mean of the observed values. Preliminary analysis of Session 1 data revealed significant performance differences from the first (Session 1A) to the second experimental block (Session 1B) at each of the four ISIs [F(1,18) ¼ 12.90, p50.01, p2 ¼ 0.42]. Rather than

There was no significant effect of block (A, B) on the late PN component at any experimental session (1, 2, 3, 4) and ERP results were, therefore, analysed as an average of the two blocks at each session. Two-way repeated measures ANOVAs with ISI (2.4, 2.0, 1.6, 1.2 seconds) and Session (1, 2, 3, and 4) as within-subjects factors and Group (mTBI and control) as a between-subjects factor were conducted to investigate the effects of practice on the mean amplitude and peak latency of the late PN component. Where Mauchly’s test of sphericity was violated, Grennhouse-Geisser corrections were again applied. There was no significant effect of ISI [F(3,54) ¼ 0.22, p ¼ 0.89, p2 ¼ 0.01], session [F(3,54) ¼ 0.17, p ¼ 0.92, p2 ¼ 0.01] or group [F(1,18) ¼ 0.12, p ¼ 0.74, p2 ¼ 0.01] on the peak latency. Amplitude of the late PN component was not affected by ISI [F(3,54) ¼ 0.85, p ¼ 0.47, p2 ¼ 0.05]. However, as seen in the interval estimates of Figure 1, mean amplitude of the late

Results Neuropsychological tests

DOI: 10.3109/02699052.2014.976273

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Figure 1. Control and mTBI group 95% confidence intervals for mean amplitude of the Late PN component measured at Fz across the four experimental sessions. Non-overlapping intervals represent statistically significant differences.

Figure 2. Sessions 1 and 4 Control (grey line) vs. mTBI (black line) group grand averaged ERP waveforms at Fz elicited in response to PASAT stimuli collapsed across ISI.

PN component was affected by practice [F(3,54) ¼ 7.27, p50.01, p2 ¼ 0.29]. Although late PN amplitude differences appeared to emerge as early as the second session, the overall effect of group just failed to reach significance [F(1,18) ¼ 4.00, p ¼ 0.06, p2 ¼ 0.18]. However, the Session  Group interaction had a significant effect on mean amplitude of late PN [F(3,54) ¼ 3.77, p ¼ 0.02, p2 ¼ 0.17]. Bonferroni corrected paired-samples t-tests (p50.0167) indicated a significant reduction in the mean amplitude of the late PN component in the control group from Session 3 to 4, t(9) ¼ 3.56, p ¼ 0.01, Session 3 95% CI [2.31, 1.61], Session 4 95% CI [2.11, 4.09]. There were no significant changes over sessions in the mean amplitude of the late PN component in the mTBI group [Session 1 to 2: t(9) ¼ 0.50, p ¼ 0.63; Session 2 to 3: t(9) ¼ 0.35, p ¼ 0.74; Session 3 to 4: t(9) ¼ 1.30, p ¼ 0.23] (see Figure 2).

Discussion Typically, the association between cognitive effort and behavioural performance is viewed as a direct relationship, such that, the greater the effort applied, the better the resulting performance. However, the dual-process theory [6] proposes

that training of a consistent set of task demands can reverse this relationship. In the current study, healthy control participants demonstrated this practice effect on the PASAT in the form of significant increases in task accuracy and attenuation of the late PN marker of executive attentional control from the ERP waveform. Despite participating in the same training regime and in spite of equivalent improvements in task accuracy, participants with mTBI did not appear to experience an easing of executive attentional demands following consistent PASAT practice. This electrophysiological abnormality was also associated with persistent selfreported post-concussion symptomatology. The capacity to benefit from practice may, therefore, be disrupted by mTBI, as performance appears to remain closely related to the degree of effort applied. The validity of such claims depends heavily on methodological issues, including the sample of participants with mTBI recruited, how mTBI history was defined and the sensitivity of the outcome measures selected [49]. Retrospective selfreport is used extensively to establish a diagnosis of mTBI [50], as individuals do not often seek medical attention at the time of injury [51, 52]. Concerns with the validity and reliability of self-report have been raised in survivors of more

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severe TBI, as they may lack insight into their disabilities [53]. Likewise, secondary gain may influence the accuracy of self-report [54, 55]. However, decreased self-awareness is not common after mTBI [56] and over-reporting rather than under-reporting would be the issue of concern in the current study. Secondary gain from over-reporting cannot be ruled out, but has traditionally been associated with claims of persisting disability and handicap requiring attention from a range of healthcare professional over many years [57]. However, symptom validity screening raised no motivation concerns in any participants with mTBI and those involved in litigation were excluded. Additionally, the terminology (e.g. concussion, head injury) used to elicit self-report can be interpreted differently from respondent to respondent [58]. During screening for study inclusion non-shared terminology was, therefore, avoided and clarification of what constitutes loss of consciousness and post-traumatic amnesia was provided by the interviewer, trained in the definition, symptoms and course of TBI [59]. Finally, misattribution of symptoms should also be considered. Post-concussion symptomatology is non-specific and overlaps with a number of other health conditions, including depression, PTSD, migraine or chronic pain [60, 61]. However, in the current study individuals with a history of illness were excluded and inclusion relied on an explicit case definition for mTBI incorporating loss of consciousness and post-traumatic amnesia [35], with all participants reporting at least one of these pathognomonic signs of brain trauma [62, 63] and 70% reporting both [64]. The current study also utilized a well-regarded, commonly used, standardized neuropsychological measure of functioning, developed for use in populations with mTBI [15–19]. To minimize the impact of potentially confounding factors, the mTBI group was matched with healthy controls on gender, age and years of education. The two groups did not differ in terms of estimated pre-morbid IQ, level of effort, mathematical ability or current mood state, all of which were within normal ranges. The mean age at time of injury was 20.21 years (range ¼ 17–29), which compares well with the age range identified in previous studies as encompassing the peak incidence of injury [65–67]. Males were slightly over-represented in the current sample, reflecting the pattern of incidence reported in previous epidemiological studies [65, 66]. The leading cause of injury in the current sample was sporting injuries, consistent with other studies of head injury in university-age populations [67, 68]. PASAT practice effects in healthy controls The current study replicates and extends previous findings regarding ERP-related PASAT practice effects [25]. In a sample of healthy control participants, the mean number of correct PASAT responses again significantly improved with practice. Behavioural improvements were again associated with significantly reduced late PN component amplitude. Consistent with PASAT research literature [17, 23, 25], the greatest changes in behavioural performance in healthy control participants occurred over preliminary sessions. Specifically, performance significantly improved from Session 1A to 1B and from Session 1B to 2. While

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performance continued to improve thereafter, differences failed to reach levels of significance, most likely due to a ceiling effect [23]. In previous work [25] continuous EEG was simultaneously recorded during only experimental Sessions 1 and 4. Hence, the time point at which significant reductions in amplitude of the late PN component occurred could not be firmly established. To resolve this issue, continuous EEG was recorded during each experimental session of the current study. Schneider and Shiffrin [6] postulated that attentional demands will be eased after an ‘appreciable amount’ of consistent training, while Logan [69] argued that practice effects can develop after a single training session. In the current study, late PN amplitude in healthy control participants appeared to begin to reduce from experimental Session 2 to experimental Session 3. However, the reduction in amplitude did not reach statistical significance until Session 4, by which time the participants had engaged in 32 trials of the task and would have performed the mental computations underlying PASAT performance nearly 500 times. These findings are in keeping with Schneider and Shiffrin’s position that the easing of attentional demands requires an extended amount of training. PASAT practice effects after mTBI In addition to advancing understanding of practice-mediated neural plasticity in information processing that occurs in healthy adults, the current study has provided insight into how these processes might be disrupted after mTBI. Unexpectedly, PASAT behavioural results did not differentiate participants with mTBI from matched healthy controls and initial testing sessions detected no abnormalities in the timing or intensity of any of the sensory or cognitive components of the ERP waveform following mTBI. In general, the results from the initial testing sessions supported the notion that the overall effect of mTBI on neuropsychological function typically recedes to non-significance within a few months post-injury [2, 18]. A possible explanation is that, because the participants with mTBI had all recovered from their injuries sufficiently to be attending university, the sample may have been biased toward individuals who had sustained only very mild, readily reversible injuries. However, there were signs the participants with mTBI had not made a complete recovery from their injuries, as they reported suffering from more intense and more prolonged symptoms of impaired concentration and headache. Additional group differences emerged when examining the unique electrophysiological data on the effects of practice. In the mTBI group there was no reliable evidence of attenuation of late PN following extended training on the PASAT task. According to connectionism [70, 71], cognitive processes, including attention, arise from parallel interactions in multiple nodes of a neural network [71, 72]. Information is not stored, represented or manipulated in any specific node of the network, but rather in the pattern of inter-connections of any number of nodes. Practice increases the efficiency of the system by strengthening associations between the input and output connections of a processing network. Following the

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DOI: 10.3109/02699052.2014.976273

consistent execution of a processing operation, executive attentional control can gradually be withdrawn, as a permanent set of associative connections facilitating the processing of an input and the retrieval of a routine output operation are established. Consequently, injury-related damage to a specific node would not be expected to result in the loss of a specific piece of knowledge, although it might make information processing within the entire network more difficult and less efficient [70]. Diffuse axonal injury occurring as a result of mTBI may, therefore, contribute to attentional dysfunction by interrupting the conduction pathways between cortical areas, reducing the efficiency of operation of the global workspace and interfering with the strengthening of associations between conceptual nodes of temporarily established processing networks [73]. It is, therefore, suggested that individuals who have sustained a mTBI are not generally incapable of dealing with non-routine situations, only that they profit less from repeated learning experiences. Nevertheless, over each experimental session the mTBI group achieved accuracy rates on the PASAT equivalent to matched healthy controls. That PASAT behavioural performance failed to discriminate the mTBI group from healthy controls was not expected. However, these findings are consistent with the argument that outcome following mTBI represents behavioural adaptation rather than recovery [32, 68]. Accordingly, residual impairment often goes undetected, as the individual is able to compensate for injury-related functional loss by increasing their reliance upon remaining information processing resources. In the current mTBI group protracted reliance on executive attentional systems appeared to serve as a compensatory mechanism which acted to limit the impact of mTBI on PASAT behavioural performance. While following extended training such a coping mechanism would not have facilitated more efficient use of processing capacity, it may allow for the executive routines or overall performance strategy to improve with repeated practice. Given the intact behavioural performance of the mTBI group, the functional implications of a diminished electrophysiological practice effect are unclear. However, the ability to automatically process some or all components of a task may be an essential mechanism of selective attention, as it allows for the reallocation of limited attentional resources. Extended reliance on executive attention strategies is likely to create a situation where cognitive operations are experienced as more effortful, as even the least demanding tasks may now engage the majority of available processing resources. Functional measures that provide an index of the intensity of cognitive activity underlying task performance may, therefore, be more likely to reveal discrepancies relative to healthy controls. The current ERP findings suggesting abnormal expenditures of cognitive effort may also provide an explanation for the persistent constellation of symptoms composing the post-concussion syndrome so frequently selfreported in the mTBI literature [3–5]. Finally, analysis of ERP data in the current study was restricted to examination of patterns of activation. However, the coping hypothesis [74] proposes that compensatory behaviour following TBI may also take the form of alternative sources of activation. Specifically, in the current study

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individuals with mTBI may have achieved normal levels of performance on the PASAT via not only sustained reliance on processes reflected in the late PN component, but through the recruitment of alternative processing structures. Although the late PN component had a frontal distribution in both experimental groups, determination of the specific cerebral source of the late PN component requires further investigation with techniques possessing greater spatial resolution.

Conclusions This study is among the first to investigate practice effects on the performance of individuals with mTBI and suggests that repeat assessment with functional ERP measures may be more sensitive than single session behavioural investigations in detecting impairment. These preliminary results provide additional evidence that recovery following mTBI may represent a functional adaptation rather than a return to premorbid levels of functioning. However, further study is required to fully clarify the repercussions of such compensatory behaviour.

Declaration of interest The authors report no conflicts of interest. This work was supported by a University of Western Australia International Postgraduate Research Scholarship awarded to the first author.

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