Dual Task Performance after Severe Diffuse Traumatic Brain Injury or Vascular Prefrontal Damage

Neuropsychologia 42 (2004) 1260–1268

Divided attention and mental effort after severe traumatic brain injury Philippe Azouvi a,∗ , Josette Couillet a , Michel Leclercq b , Yves Martin c , Sybille Asloun a , Marc Rousseaux d a

Service de Rééducation Neurologique, Formation de Recherche Claude Bernard, Faculté de Médecine Paris-Ile de France Ouest, Université de Versailles-Saint Quentin, Hˆopital Raymond Poincaré, Garches 92380, France b Centre Neurologique William Lennox, Ottignies Louvain-la-Neuve, Belgique, France c Centre de Rééducation l’Espoir, Lille-Hellemmes, France d Service de Rééducation Neurologique, Hˆ opital Swynghedauw, Lille, France Received 22 July 2003; received in revised form 5 January 2004; accepted 7 January 2004

Abstract The aim of this study was to assess dual-task performance in TBI patients, under different experimental conditions, with or without explicit emphasis on one of two tasks. Results were compared with measurement of the subjective mental effort required to perform each task. Forty-three severe TBI patients at the subacute or chronic phase performed two tasks under single- and dual-task conditions: (a) random generation; (b) visual go–no go reaction time task. Three dual-task conditions were given, requiring either to consider both tasks as equally important or to focus preferentially on one of them. Patients were compared to matched controls. Subjective mental effort was rated on a visual analogic scale. TBI patients showed a disproportionate increase in reaction time in the go–no go task under the dual-task condition. However, they were just as able as controls to adapt performance to the specific instructions about the task to be emphasised. Patients reported significantly higher subjective mental effort, but the variation of mental effort according to task condition was similar to that of controls. These results suggest that the divided attention deficit of TBI patients is related to a reduction in available processing resources rather than an impairment of strategic processes responsible for attentional allocation and switching. The higher level of subjective mental effort may explain why TBI patients frequently complain of mental fatigue, although this subjective complaint seems to be relatively independent of cognitive impairment. © 2004 Elsevier Ltd. All rights reserved. Keywords: Divided attention; Central executive; Working memory; Executive functions; Traumatic brain injury

1. Introduction Survivors from a severe traumatic brain injury (TBI) frequently have difficulty performing more than one thing at a time (dual-task performance, or divided attention). This difficulty has been found to be significantly correlated with the inability to return to work (Crépeau & Scherzer, 1993; Van Zomeren & Van den Burg, 1985; Vilkki et al., 1994) or with dependency in complex activities of daily living (Brouwer, Withaar, Tant, & Van Zomeren, 2002; Withaar, 2000). Although a large number of studies have been conducted to understand this disorder, its nature remains the subject of debate (for a review, see Leclercq & Azouvi, 2002; Van Zomeren & Brouwer, 1994). The brain and cognitive mechanisms underlying dual-task performance are still poorly understood. The co-ordination of two different tasks is usually considered as one of the key ∗

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0028-3932/$ – see front matter © 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2004.01.001

functions of the central executive system within Baddeley (1986) working memory model, or alternatively of the supervisory system within Shallice (1988) model of executive attentional control. However, the relationships of dual task processing with other aspects of executive functioning remain to be elucidated. For example, Miyake, Friedman, Emerson, Witzki, and Howerter (2000) recently studied the performance of healthy individuals on a set of executive tasks, that were each assumed to predominantly tap one of three basic domains associated with executive functioning, i.e. mental set shifting, information updating and monitoring, and inhibition of prepotent responses. They found that dual-task performance was not significantly related to any of these three basic executive domains, suggesting that dual tasking may tap an executive function that is somewhat independent of the three target functions examined in this study. Also, the neural basis of dual-task processing remains unclear, and functional neuro-imaging studies have yielded contradictory results regarding the involvement of the prefrontal cortex (Adcock,

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Constable, Gore, & Goldman-Rakic, 2000; D’Esposito et al., 1995). Experimental studies on divided attention after traumatic brain injury have produced contrasting results. Early studies found no additional deficit in divided attention when speed of processing was controlled for (Brouwer, Ponds, Van Wolffelaar, & Van Zomeren, 1989; Spikman, van Zomeren, & Deelman, 1996; Veltman, Brouwer, van Zomeren, & van Wolffelaar, 1996). Conversely, more recent studies showed that, even after experimental or statistical control for slowed processing, severe TBI patients still demonstrated a significant dual-task decrement (McDowell, Whyte, & D’Esposito, 1997; Stablum, Leonardi, Mazzoldi, Ulmita, & Morra, 1994; Vilkki, Virtanen, Surma-Aho, & Servo, 1996). These discrepancies could result from the different attentional demands within the individual tasks that were used (Leclercq & Azouvi, 2002). For example, Park, Moscovitch, and Robertson (1999) investigated the interaction between divided attention and working memory load, and found that dual-task performance of severe chronic TBI patients was significantly impaired under a condition including a significant working memory load, requiring controlled processing, while performance was at the level of controls when the tasks could be carried out relatively automatically. Convergent findings have been recently reported by Brouwer and colleagues (Brouwer, Verzendaal, van der Naalt, Smit, & Van Zomeren, 2001; Brouwer et al., 2002; Withaar, 2000). In these latter studies, TBI patients had to perform dual tasks under different conditions, using different difficulty levels (Brouwer et al., 2002; Withaar, 2000), or different degrees of dependency between the subtasks (Brouwer et al., 2001). A divided attention deficit was found only in the more demanding conditions. In addition, dual-task measures under the most difficult condition showed the highest correlations with performance in daily-living activities, thus suggesting the ecological validity of divided attention performance under high time-pressure (Withaar, 2000). Similar results were found in divided attention studies performed in our department (Azouvi, Jokic, Van der Linden, Marlier, & Bussel, 1996; Leclercq et al., 2000). In a first study using a dual-task paradigm performed without time-pressure and which required little executive control, we found no disproportionate dual-task impairment in the TBI group (Azouvi et al., 1996). However, in two other experiments under more demanding conditions (either because of time-pressure or because of higher task complexity), TBI patients showed a significant impairment in dual-task processing (Azouvi et al., 1996; Leclercq et al., 2000). The suggestion that deficits in divided attention after TBI are task-dependent is also in accordance with a meta-analysis carried out by Park et al. (1999), who found that the severity of the dual-task decrement varied considerably from one study to another (range: 0.03–1.28). Although slowed information processing seems sufficient to explain a divided attention deficit in simple and relatively automatic dual tasks, additional impairment emerges in more complex tasks, performed

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under high time-pressure, or including substantial working memory load, or requiring executive control. The present study had three main objectives: (1) To re-address the question of divided attention, and to extend findings of a previous study (Leclercq et al., 2000) in a larger sample of patients and with a more complex task. (2) To assess more precisely the ability of patients to allocate attentional resources to one or the other of two competing tasks. Patients were asked alternatively to put emphasis on one task or on the other. If the divided attention deficit is related to an impairment of control processes implicated in switching or allocating attentional resources, patients should have more difficulty than controls to adapt their performance according to task instructions; in contrast, if the divided attention deficit is related to a reduction of available resources, they should have no additional problem in the emphasised dual tasks. (3) To investigate the relationship between divided attention and mental effort. Indeed, fatigue is a frequent complaint of TBI patients, which has received little attention in the literature. Fatigue could be assumed to be a consequence of overwhelming efforts made to compensate for cognitive limitations. If this is the case, the dual-task condition should be accompanied by a disproportionate increase in the subjective mental effort in the TBI group. 2. Methods 2.1. Participants Forty-three severe TBI patients (11 women and 32 men) were selected for this study. They were consecutively recruited in the rehabilitation units to which they had been referred for evaluation and/or treatment. Inclusion criteria were the presence of a severe high velocity closed-head TBI, with the lowest post-resuscitation Glasgow Coma Score (GCS) of eight or less. Exclusion criteria were the presence of aphasic disorders, and motor deficit on the dominant upper limb which might have impaired manipulation of the response device. Patients with previous neurological or psychiatric disease, or with known substance abuse, were also excluded. They were all out of post-traumatic amnesia, as assessed by a score of 76 or more at the Galveston Orientation and Amnesia Test (Levin, O’Donnell, & Grossman, 1979). Mean age was 26.7 (S.D.: 8.9), and mean education duration 11.0 years (S.D.: 2.6). The mean lowest GCS score was 5.6 (S.D.: 1.4, range: 3–8), coma duration was 16.3 days (S.D.: 11.4, range: 1–50) and PTA duration 57.9 days (S.D.: 48.5, range: 6–80) (data on injury severity were not available in six cases). They were in a subacute/chronic stage (mean time since injury: 9.6 months, S.D.: 11.1, range: 1–50). Patients were compared with a group of 42 healthy individuals, matched for age, gender and education duration (mean age: 26.6 years, S.D.: 9.4; mean education duration: 11.3 years, S.D.: 2.4). A simple baseline neuropsychological assessment focusing on executive functions and working memory was given

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Table 1 Baseline neuropsychological and behavioural assessment TBI Forward digit span Backward digit span Fluency (animals) Fluency (P) DEX (n = 23)

6.1 4.7 21.3 13.3 25.8

(1.3) (1.3) (7.3) (5.6) (11.7)

Controls

P-value

6.2 4.9 32.4 25.3

0.6 0.4 0.1). These results are illustrated in Figs. 1–3, showing that TBI patients performed more slowly than controls in both the go–no go and the randomisation task, and that their RQ was poorer than that of controls. The significant main effect of condition, that was found with all measures of performance, was indeed related to poorer performance under dual-task conditions, in both groups. To further assess the significant group by condition interaction in the go–no go task, an additional analysis was computed, using dual-task decrement measures. For this purpose,

Reaction Time (msec) 1100 1000 900 800 Controls TBI

700 600 500 400 300 single task

dual task (random generation) dual task (no emphasis) dual task (go-no go)

Fig. 1. Mean (±1 S.E.) RT under single- and dual-task conditions.

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Randomisation quotient 110 107,5 105 102,5 100 Controls TBI

97,5 95 92,5 90 87,5 85 single task

dual task (random generation) dual task (no emphasis) dual task (go-no go)

Fig. 2. Mean (±1 S.E.) RQ under single- and dual-task conditions.

ratios of the dual-task to single task RT were computed, for the three different dual-task conditions (emphasised and non-emphasised). A 2 (groups) × 3 (dual-task instructions: no-emphasis versus emphasis on random generation versus emphasis on go–no go) repeated measures ANOVA was then computed, with the dual-task decrement as dependent variable. This analysis showed a significant main effect of group (F(1, 80) = 6.7, P < 0.02), a significant main effect of instruction (F(2, 160) = 16.9, P < 0.0001), but with-

out any significant interaction (F(2, 160) = 1.0, P > 0.1). These results are illustrated in Fig. 4, showing that the dual task decrement was higher in the patient than in the control group, but varied in a parallel way in both groups according to task instructions. Indeed, the dual-task decrement in the go–no go task was higher in both groups when emphasis was set on random generation. In addition, to obtain a better understanding of patients’ performance in the randomisation task, each individual

Randomisation duration (secs) 260 240 220 200 Controls

180

TBI

160 140 120 100 single task

dual task (random generation) dual task (no emphasis) dual task (go-no go)

Fig. 3. Mean (±1 S.E.) randomisation duration under single- and dual-task conditions.

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Dual-task decrement (go-no go task) 2,5 2,25 2 1,75 Controls

1,5

TBI

1,25 1 ,75 ,5 no emphasis

emphasis:RNG

emphasis:go-no go

Fig. 4. Mean (±1 S.E.) dual-task decrement, as defined as the ratio of the dual-task to single-task RT for the three dual tasks.

randomness index was analysed separately. A significant main effect of group was found for all indexes: triplets (F(1.82) = 3.9, P = 0.05), number of phases (F(1.82) = 9.1, P < 0.01), the mean successive difference (F(1.81) = 7.4, P < 0.01), χ2 (F(1.82) = 5.1, P < 0.05), Evans randomisation index (F(1, 82) = 3.9, P = 0.05), and autocorrelation index (F(1.82) = 7.5, P < 0.01). 3.2. Subjective mental effort Analysis of mental effort used a 2 (groups) × 2 (tasks: random generation versus go–no go) × 4 (experimental conditions) repeated measures ANOVA. This analysis revealed

a significant main effect of group (F(1, 79) = 6.7, P < 0.02), a significant main effect of task (F(1, 79) = 47.9, P < 0.0001), and a significant main effect of experimental condition (F(3, 237) = 13.9, P < 0.0001). Only the task × condition interaction was significant (F(3, 237) = 8.2, P < 0.0001). All other interactions were non significant (all Ps > 0.1), including the group × condition interaction, that did not even approach statistical significance (F(3, 237) = 0.1, P = 0.9). These results are illustrated in Fig. 5, showing that rating of subjective mental effort was systematically higher in the patient group. The main effect of task was related to higher ratings of mental effort for the randomisation than for the go–no go task, and the significant

Fig. 5. Mean (±1 S.E.) subjective mental effort devoted to each task under the four experimental conditions.

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task × condition interaction to the fact that the difference between mental effort in both tasks was higher under dualthan under single-task condition. However, the absence of interaction with the group indicated that, although patients reported higher levels of mental effort, subjective mental effort varied according to the task and to the experimental condition in a similar way in both groups. In addition, Spearman rank correlation coefficients were computed between performance and subjective mental effort on each individual task, both under dual- and single-task conditions. Most of these correlations (10 out of 12) were low and did not reach statistical significance. Mental effort was also found to be poorly correlated with dual-task decrement and with time since injury.

4. Discussion The aim of the present study was to address the question of divided attention and of subjective mental effort at a subacute/chronic stage after a severe to very severe TBI. Three dual-task conditions were used, one requiring subjects to pay the same amount of attention to each individual task, and the two others requiring special focusing either on one task or on the other. In accordance with previous studies (Azouvi et al., 1996; Brouwer et al., 2001; Brouwer et al., 2002; McDowell et al., 1997; Park et al., 1999; Stablum et al., 1994; Vilkki et al., 1996; Withaar, 2000), and particularly with a recent study using a quite similar methodology (Leclercq et al., 2000), patients demonstrated a disproportionate dual-task decrement, in comparison with controls. Indeed, the dual-task to single-task RT ratio was significantly higher in the patient group, whatever the dual-task condition. This finding confirms previous findings showing that severe TBI patients have difficulty in dealing with two simultaneous tasks, at least if these tasks require some degree of executive control (Leclercq & Azouvi, 2002; Park et al., 1999). In addition, we also confirmed our previous finding (Leclercq et al., 2000) that TBI patients showed a significantly higher dual-task decrement in the RT task only, and not in random generation, this suggesting that they tended to spontaneously emphasise random generation, which may be assumed to require a higher level of attentional control. However, an original finding of the present study was that, although TBI patients had more difficulty than controls in dealing with two tasks simultaneously, they were able, just as well as controls were, to allocate available attentional resources to one task or the other, according to task instructions. Brouwer et al. (1989) found quite similar results using a different paradigm, but in that study, TBI patients did not show any significant divided attention deficit. These results raise questions about the mechanisms of the divided attention deficit after TBI. The ability to divide attention has repeatedly been considered as a key function of the central executive system of working memory (Baddeley & Hitch, 1974) or of the supervisory system of Shallice

(1988) model. However, the precise cognitive and neural basis of divided attention remains unclear. Neuro-imaging studies of divided attention have yielded contradictory results (Collette & van der Linden, 2002). Some studies found that dual-task performance needs additional cortical activity in regions not activated by the individual tasks, particularly in the dorsolateral prefrontal cortex (D’Esposito et al., 1995; Herath, Klingberg, Young, Amunts, & Roland, 2001; Koechlin, Basso, Pietrini, Panzer, & Grafman, 1999). In contrast, others found that dual-task performance only extends and enhances activity in regions already activated by the single tasks, and does not recruit additional areas (Adcock et al., 2000; Klingberg, 1998). Nevertheless, it is generally acknowledged that diffuse brain damage, such as that associated with TBI or Alzheimer’s disease, is associated with a divided attention deficit. The neural basis of attentional deficits after TBI are not yet fully understood. A recent study using Positron Emission Tomography showed that cognitive and behavioural deficits after severe TBI were associated with a reduced activity of an executive-attentional network, including the prefrontal and cingulate areas (Fontaine, Azouvi, Remy, Bussel, & Samson, 1999). In the present study, TBI patients showed a significantly disproportionate dual-task decrement, but a preserved ability to preferentially allocate attentional resources to one task or the other according to task instructions. These findings support the assumption that limitations in divided attention after TBI are related to a reduction in available processing resources rather than to an impairment of strategic processes responsible for attentional allocation and switching between tasks. Subjects were asked to rate their subjective mental effort on each individual task. TBI patients reported significantly higher effort ratings than controls, whatever the task and the experimental condition. This suggests that they had to engage more effort on a given task, even in a relatively easy condition. Both groups reported more mental effort for the randomisation than for the go–no go task. Such a finding supports the assumption that random generation is more complex and requires a higher level of mental control. Increased mental effort might be assumed to result in increased fatigue in the TBI group. Indeed, fatigue is a very frequent and long-lasting complaint after TBI. For example, Brooks, Campsie, Symington, Beattie, and MacKinlay (1986) found that 62% of the relatives of severely injured patients reported tiredness 5 years after the injury. Similarly, fatigue was reported by 72% of patients 2 years post-injury in an Australian study (Ponsford, Olver, & Curran, 1995). Fatigue has received little attention in TBI research, probably because it is difficult to measure objectively. According to van Zomeren, Brouwer, and Deelman (1984), fatigue could be due to the constant compensational effort required to cope with the demands of everyday life. Riese et al. (1999) used both psychophysical and subjective measures of mental effort in a group of severe TBI patients performing a long-lasting dual task, and found higher psychophysiological cost and subjective distress, which could be related to

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mental fatigue. The findings from the present study were in accordance with this assumption. If TBI patients have to produce higher levels of mental effort, this may be assumed to have both a psychological and physiological cost, which may be subjectively experienced as a sensation of fatigue. However, contrary to expectations, patients were able to adapt their mental effort according to task requirements as efficiently as controls, although at a higher level. In addition, effort rating poorly correlated with performance in tests or dual-task decrement. This suggests that the subjective perception of effort is not directly related to cognitive impairment, although it may be assumed that reduced ability to engage attentional resources could indirectly affect patients’ efficiency on complex and long-lasting tasks. In conclusion, the present study confirms that severe TBI impairs the ability to deal simultaneously with two different tasks, at least when these tasks put a significant load on working memory and/or executive control. In addition, our data support the assumption that the divided attention deficit is mainly related to a reduction in available processing resources rather than to an impairment of strategic processes responsible for allocation of attention and task switching. Finally, it was found that TBI patients needed a higher level of subjective mental effort to perform the tasks. However, subjective mental effort did not seem to be related to task difficulty or to performance. This may explain why fatigue is such a pervasive problem after TBI, as it may interfere with performance in even relatively simple and automatic tasks. References Adcock, R. A., Constable, R. T., Gore, J. C., & Goldman-Rakic, P. S. (2000). Functional neuroanatomy of executive processes involved in dual task performance. Proceedings of the National Academy of Science of the USA, 97, 3567–3572. Azouvi, P., Jokic, C., Van der Linden, M., Marlier, N., & Bussel, B. (1996). Working memory and supervisory control after severe closed head injury. A study of dual task performance and random generation. Journal of Clinical and Experimental Neuropsychology, 18, 317–337. Baddeley, A., & Hitch, G. (1974). Working memory. In G. A. Bower (Ed.), Recent advances in learning and motivation (Vol. 8, pp. 47–90). New York: Academic Press. Baddeley, A. D. (1986). Working memory. New York: Oxford University Press. Brooks, D. N., Campsie, L., Symington, C., Beattie, A., & MacKinlay, W. (1986). The five year outcome of severe blunt head injury: A relative’s view. Journal of Neurology, Neurosurgery and Psychiatry, 49, 764–770. Brouwer, W. H., Ponds, R. W. H. M., Van Wolffelaar, P. C., & Van Zomeren, A. H. (1989). Divided attention 5 to 10 years after severe closed head injury. Cortex, 25, 219–230. Brouwer, W. H., Verzendaal, M., van der Naalt, J., Smit, J., & Van Zomeren, A. H. (2001). Divided attention years after severe closed head injury: The effect of dependencies between the subtasks. Brain and Cognition, 46, 54–56. Brouwer, W. H., Withaar, F. K., Tant, M. L. M., & Van Zomeren, A. H. (2002). Attention and driving in traumatic brain injury: A question of coping with time-pressure. Journal of Head Trauma Rehabilitation, 17, 1–15.

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