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Neuropsychological Rehabilitation: An International Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/pnrh20
Modularity in rehabilitation of working memory: A single-case study ab
bc
Claire Vallat-Azouvi , Pascale Pradat-Diehl
&
bde
Philippe Azouvi a
UGECAM-antenne UEROS-SAMSAH 92, Raymond Poincare hospital, Garches, France b
ER 6, UMPC, Paris, France
c
AP-HP, Salpétrière hospital, Department of Physical Medicine and Rehabilitation, Paris, France d
AP-HP, Raymond Poincare hospital, Department of Physical Medicine and Rehabilitation, Garches, France e
EA 4047, University of Versailles-Saint Quentin, France Published online: 19 Feb 2014.
To cite this article: Claire Vallat-Azouvi, Pascale Pradat-Diehl & Philippe Azouvi (2014) Modularity in rehabilitation of working memory: A single-case study, Neuropsychological Rehabilitation: An International Journal, 24:2, 220-237, DOI: 10.1080/09602011.2014.881294 To link to this article: http://dx.doi.org/10.1080/09602011.2014.881294
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Neuropsychological Rehabilitation, 2014 Vol. 24, No. 2, 220– 237, http://dx.doi.org/10.1080/09602011.2014.881294
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Modularity in rehabilitation of working memory: A single-case study Claire Vallat-Azouvi1,2, Pascale Pradat-Diehl2,3, and Philippe Azouvi2,4,5 1
UGECAM-antenne UEROS-SAMSAH 92, Raymond Poincare hospital, Garches, France 2 ER 6, UMPC, Paris, France 3 AP-HP, Salpe´trie`re hospital, Department of Physical Medicine and Rehabilitation, Paris, France 4 AP-HP, Raymond Poincare hospital, Department of Physical Medicine and Rehabilitation, Garches, France 5 EA 4047, University of Versailles-Saint Quentin, France (Received 13 June 2013; accepted 13 January 2014)
The objective of the present study was to assess the specificity of rehabilitation on different subdomains of working memory. A 38-year-old female with chronic (4 years) stroke suffered from an impairment of the three subdomains of working memory (modality-specific storage systems for verbal and visuo-spatial information and the central executive). She was given an experimental rehabilitation programme, using a multiple-baseline across behaviour design. After two baseline measures three months apart, the first training stage focused on the phonological loop, the second on the visuo-spatial sketchpad, and the third on central executive functions. Verbal aspects of working memory improved significantly after the first training stage, while visuo-spatial tests improved after the second training stage. Central executive functions improved mainly after the third training stage. Modularity effects were not as pronounced for less specific ecological outcome measures, such as the Working Memory Questionnaire, which improved throughout the trial, irrespective of the training condition. This case study suggests that there are both domain-specific and generalisation effects in rehabilitation of working memory, and that rehabilitation should be adapted and tailored to each individual patient’s impairments. Correspondence should be addressed to Claire Vallat-Azouvi, PhD, Antenne UEROSSAMSAH 92-UGECAM, Hoˆpital Raymond Poincare´, 92380 Garches, France. E-mail: claire. [email protected] # 2014 Taylor & Francis
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Keywords: Working memory; Rehabilitation; Stroke; Modularity; Cognition.
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INTRODUCTION Working memory is a complex system involved in short-term storage and simultaneous processing of information (Baddeley, 2003). This function, which is of great importance in many cognitive tasks, may be impaired in several neurological conditions, such as stroke (Wright & Shisler, 2005), traumatic brain injury (Vallat-Azouvi, Weber, Legrand, & Azouvi, 2007), Alzheimer’s disease (Baddeley, Baddeley, Bucks, & Wilcock, 2001), or in children with attention deficit hyperactivity disorder (ADHD) (Martinussen, Hayden, Hogg-Johnson, & Tannock, 2005). Current theoretical and neuro-anatomical models of working memory suggest that it relies on at least two distinct modality-specific storage systems, and on a multimodal controlling function. The modality-specific storage systems are usually referred to as the phonological loop (for verbal information) and the visuo-spatial sketchpad (for visual and spatial information), while the multimodal controlling and coordinating system has been called the central executive, or controlled or executive attention (Baddeley, 2003; Engle, 2002). Recent group and single-case studies suggest that intensive training may improve working memory in patients suffering from stroke (Lundqvist, Grundstrom, Samuelsson, & Ronnberg, 2010; Vallat et al., 2005; Westerberg et al., 2007), traumatic brain injury (Couillet et al., 2010; Serino et al., 2007; Vallat-Azouvi, Pradat-Diehl, & Azouvi, 2009), brain tumour (Duval, Coyette, & Seron, 2008), and in children with ADHD (Holmes, Gathercole, & Dunning, 2009; Klingberg et al., 2005; Klingberg, Forssberg, & Westerberg, 2002; Martinussen et al., 2005). Adapted and extended training has also been found to enhance working memory capacity in healthy individuals, associated with changes in brain activity in frontal and parietal cortex and basal ganglia (Jaeggi, Buschkuehl, Jonides, & Perrig, 2008; Olesen, Westerberg, & Klingberg, 2004; Westerberg & Klingberg, 2007), although conflicting results have been reported (Redick et al., 2013) (for a recent review see Klingberg, 2010). However, most studies used either one single training task, or a combination of tasks given to all patients in a similar way. To our knowledge, there has not been any attempt to disentangle the effect of training on the various subcomponents of working memory. The only exception was the study by Duval et al. (2008), but these authors used a different theoretical framework, and trained successively the following three sub-components of the central executive: processing load, updating and dual-task monitoring. The programme proved to be effective for all three working memory components, but the specificity of training was limited.
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The issue of specificity of training is important in two aspects. First, from a theoretical point of view, if training effects are domain-specific, this supports the idea that working memory components may be modular and independent in terms of processing requirements (and eventually neuroanatomical location). On the other hand, if generalisation takes place this is most probably not the case and the components of working memory might share these requirements. Second, from a clinical point of view, all patients do not show the same pattern of impairment, and it could be assumed that training should be adapted to the specific impairment of an individual patient. We present a single-case rehabilitation study of a patient with chronic left hemisphere stroke suffering from a selective impairment of working memory involving the three domains (the phonological loop, the visuo-spatial sketchpad and the central executive). Training was given in three stages, focusing successively on each one of these three domains, in order to assess the domain-specific and the generalisation effects of training within working memory.
CASE REPORT AC was a 38-year-old woman, working as assistant manager in a bank, who suffered from an ischaemic stroke in the retrorolandic part of the superficial left sylvian arterial territory. At the acute stage, she presented a severe aphasia, with mutism and bucco-facial apraxia, but preserved comprehension, except for long sentences and for written texts. Her condition improved progressively and when she was referred to our rehabilitation department, a few weeks after stroke, her language impairment was considered as characteristic of a conduction aphasia. After a few months of speech and language therapy, her language showed a very good recovery. However, despite this dramatic improvement of language abilities, she still continued to complain of difficulty in dual-task situations, and also in taking notes, concentrating, memorising information in the short-term, holding a conversation, and of mental fatigue. A comprehensive neuropsychological assessment was carried out four years and three months post stroke onset (Table 1). At this time, language, as assessed with conventional aphasia tests, had nearly fully recovered, as shown by scores at ceiling on naming, picture description, written comprehension, and syntactic comprehension tests. Long-term verbal episodic memory, reasoning, planning, flexibility and basic attentional abilities were preserved, with the exception of a moderate slowing in choice reaction time tasks. There was no sign of anxiety or depression, and the patient scored below cut-off on a depression scale. There was however a mild impairment of written text comprehension, and of both arithmetical and logical problem solving. Her verbal span was 4
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TABLE 1 First baseline neuropsychological assessment
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Tasks Language Naming (DO80)a Figure description b Syntactic oral comprehension b,c Oral comprehension (% hits) b,c Token Test (written form) d Token Test (oral form) d Written text comprehension (MT86) c Written syntactic comprehension (Rey’s 15 questions)e Calculation (EC301) f Attention (TAP)g Phasic alertness, median RT (Standard score) Flexibility, median RT (Standard score) Flexibility, errors (Standard score) Selective attention, median RT (Standard score) Selective attention, errors (Standard score) Episodic memory Complex figure recall (centile) h Word list learning (Rey, Centile) e Paired associate learning (WMS-R) i Problem solving Arithmetic problem solving (% hits) b Logic verbal problem solving b Working memory j Digit span, forward Digit span, backward Visual span, forward Visual span, backward Depression (MADRS) k
AC score/maximal score
80/80 18/18 38/38 80 36/36 29/36 6/6 15/15 92/92 55 34 46 20 44 50 75 24/24 66 4,5/6 4 4 6 4 6/60
a DO80: naming test (Deloche et al., 1997); b,caphasia batteries (Ducarne de Ribeaucourt, 1989; Nespoulous. & Roch-Lecour, 1992); dToken Test (De Renzi & Vignolo, 1962); eAuditory Verbal Learning Test (Rey, 1964); fcalculation assessment (Deloche et al., 1994) ;gTAP (Zimmermann & Fimm, 2002) (mean standard note ¼ 50, SD ¼ 10); hComplex Figure (Osterrieth, 1944); iWechsler Memory Scale–Revised (Wechsler, 1991); jWorking Memory Assessment (Vallat-Azouvi et al., ˚ sberg Depression Rating Scale (MADRS; Montgomery & Asberg, 1979). 2007); kMontgomery–A
(both forward and backward), and forward and backward visuo-spatial spans were 6 and 4, respectively, thus suggesting a working memory deficit. A more detailed assessment focusing on working memory was then given, which revealed an isolated and severe deficit of all components of working memory, including the phonological loop, the visuo-spatial sketchpad and the central executive. Central executive tasks, such as the Brown-Peterson tasks of short-term memory with interference were significantly impaired,
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in comparison with matched controls, both in the verbal and visual modalities (she was unable to maintain three items in short-term memory for 20 seconds, while simultaneously performing a resource demanding task). Detailed performance on working memory tasks will be presented later (see Results section and Tables 2 and 3). It was then decided to propose to AC a specific training of working memory, following a previously described methodology (Vallat et al., 2005; VallatAzouvi et al., 2009). However, in order to disentangle the effects of rehabilitation on the different subcomponents of working memory, training focusing on the phonological loop, the visuo-spatial sketchpad and the central executive was given separately and successively. The patient was informed of the experimental aim of the study and gave her consent to participate. Data were obtained in compliance with the Helsinki Declaration.
Experimental design A single-case multiple baseline-across behaviours design was used (Wilson, 1987). Three successive training stages were proposed. The first stage focused on training of the phonological loop, the second stage on the visuo-spatial sketchpad, and the third stage on the central executive. Although AC was at a chronic stage, to control for re-test effects, and to produce a more reliable baseline assessment, two baseline measures of different components of working memory were taken before starting training (BL1 and BL2), with a three month inter-test interval. Outcome measures were obtained just after the end of each training stage (they will be referred to as T1, T2 and T3, respectively).
Training The training tasks used in the two first stages have been described in detail in two previous papers (Vallat et al., 2005; Vallat-Azouvi et al., 2009). Training addressed both storage and processing of information in working memory. Eight tasks addressing verbal aspects of working memory were used in the first training stage (reconstitution of words from oral spelling, with or without a letter omitted, oral spelling, odd or even number of letters in a word, reconstitution of words from syllables, alphabetic way, word sorting in alphabetic order, acronyms). Four tasks addressing the visuo-spatial sketchpad were used in the second training stage (2-D mental imagery on a chessboard, 2-D mental imagery on a calculator keyboard, 3-D mental imagery, visual n-back). A description of these 12 tasks can be found in the Appendix at the end of this paper. In the last stage, focusing on central executive functions, new tasks were designed in order to tap more intensively executive aspects of working memory. These tasks (also presented in more detail in the Appendix) required simultaneous storage and processing of
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TABLE 2 Performance on PM tasks and measures of neuropsychological functioning Digit span, forward
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Controls BL1 BL2 Post-T1 Post-T2 Post-T3 Digit span, backward Controls BL1 BL2 Post-T1 Post-T2 Post-T3 Visual span, forward Controls BL1 BL2 Post-T1 Post-T2 Post-T3 Visual span, backward Controls BL1 BL2 Post-T1 Post-T2 Post-T3
2
3
100 (0.00) 100 (0.00)
4 100 (0.00)
5
6
83.27 (29.01) 63.33 (39.79)
100 100 100 100 100
80 60 100 100 100
60 60 100 100 100
0 0 100 100 100
0 0 40 40 40
2
3
4
5
6
100 (0.00) 100 (0.00) 89.87 (15.17) 66.66 (45.65) 46.66 (43.14) 100 100 100 100 100
80 60 100 100 100
40 40 100 100 100
2
3
4
100 (0.00) 100 (0.00) 96.67 (7.46)
0 0 40 40 80 5 70 (36.13)
0 0 0 0 0 6
100 80 100 100 100
80 80 100 100 100
60 60 100 100 100
40 40 80 100 100
60 40 80 100 100
2
3
4
5
6
100 (0.00) 100 (0.00) 93.33 (9.13) 100 100 100 100 100
80 60 80 100 100
40 40 40 100 100
70 (32.06) 0 0 0 40 80
7
13.33 (18.26) 3.33 (7.45) 0 0 0 20 20
16.66 (20.41) 0 0 0 0 0
BL ¼ baseline; Post-T1, T2 and T3 refer to the three post-training outcome measures.
information: n-back tasks using words or questions, and reading span tasks were used (Daneman & Carpenter, 1980). The tasks were arranged in a difficulty hierarchy order organised to follow two criteria, capacity (amount of information) and level of processing (stimulus complexity). Training was given during two one-hour sessions per week. Training stages 1 and 2 lasted six months each, and training stage 3 lasted seven months. The difficulty level was progressively adapted to the patient’s
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VALLAT-AZOUVI, PRADAT-DIEHL, AND AZOUVI TABLE 3 Verbal and visual Brown-Peterson (BP) tasks). Recall delay (sec) 5
10
100 (0.00)
100 (0.00)
BL1 BL2
16 16
16 16
0 0
Post-T1 Post-T2 Post-T3
66 83 100
83 83 100
83 83 83
5
10
20
96 (8.94)
96 (8.94)
BL1 BL2
66 66
16 16
0 0
Post-T1 Post-T2 Post-T3
33 83 100
33 50 83
50 50 83
5
10
20
100 (0.00)
96.67 (7.46)
BL1 BL2
16 16
16 16
0 0
Post-T1 Post-T2 Post-T3
33 83 83
16 83 100
16 50 83
BP- articulatory suppression
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Controls
BP-mental calculation Controls
Visual BP-with interference Controls
20 100 (0.00)
80 (24.49)
100 (0.00)
BL ¼ baseline; Post-T1, T2 and T3 refer to the three post-training outcome measures.
performance, starting at the n-1 backward digit span level. Each level was trained until the patient succeeded in 90% of the trials.
Outcome measures Four sets of outcome measures were used, including non-target measures to assess the specificity of training (see Vallat-Azouvi et al., 2009, for a more detailed presentation of the tasks). Cognitive tasks specifically designed to assess the different components of working memory. The phonological loop and the visuo-spatial sketchpad were assessed with forward and backward digit and visuo-spatial spans, respectively (five trials for each span length). The central executive was
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assessed with the Brown-Peterson paradigm, both in the verbal and visual modalities. This task requires recalling short pieces of verbal or visual information after a delay of 5, 10 or 20 seconds, while simultaneously performing a concurrent distracting task of increasing complexity. Central executive functions were additionally assessed with the 2-back and the divided attention subtasks of the Test for Attentional Performance (TAP; Zimmermann & Fimm, 2009). Non-specific tasks requiring working memory. These included tasks that were not specifically designed to assess working memory, that were not trained, but that nevertheless include a high working memory load. This subset of tasks included arithmetic problem solving (15 problems of increasing complexity), sentence comprehension (Ducarne de Ribeaucourt, 1989), the Token test (De Renzi & Vignolo, 1962), and the mental flexibility subtest of the TAP (Zimmermann & Fimm, 2009). Ecological questionnaire. The Working Memory Questionnaire (WMQ; Vallat-Azouvi, Pradat-Diehl, & Azouvi, 2012) has been designed specifically to assess everyday life difficulties related to working memory failures. It is a self-assessment questionnaire comprising 30 questions scored on a five-point Likert scale, ranging from 0 (“no problem at all”) to 4 (“very severe problem in everyday life”). It has been previously found sensitive to brain damage (Vallat-Azouvi et al., 2012). Non-target tasks. These measures were assumed not to require working memory, and were not expected to improve after therapy. Non-target measures included the following: a simple visual reaction time, from the TAP; two long-term verbal memory tasks: a word recognition task in which 30 words were presented orally to the patients, and had to be recognised 20 minutes later, mixed with 60 distractors; and a test of visual longterm memory, Complex Figure Recall (Rey, 1959). To control for re-test effects, parallel versions of the tasks were designed and outcome measures were always different from the tasks used for the therapy. To reduce as far as possible an examiner’s bias, therapy and assessment were performed by different investigators, blind one from each other. Data have been analysed by comparison of AC’s performance to that of five healthy subjects matched for age and education (three men, mean age ¼ 40 +/- 1.87 years, mean education duration ¼ 12 +/2.5 years), with the exception of outcome measures from the TAP, which were compared to the published norms for this battery (Zimmermann & Fimm, 2009).
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Data analysis
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For the main outcome measures (spans and Brown-Peterson tasks), statistical analyses were computed using Chi-2 statistics on the percentage of correct responses on the five successive testing sessions. Such analysis could not be conducted on other measures, for which data analysis relied on comparison of AC’s mean standardised scores to published norms for the tests, when available, or on visual inspection of data when norms were not available.
Results The results of cognitive tasks specifically designed to assess the different components of working memory are presented in Tables 2 and 3. Performance was stable on the two baseline measures of digit and visual spans (Table 2) and significantly improved after therapy (digit span, forward: x2 ¼ 211.03; df ¼ 16; p , .0001; digit span, backward: x2 ¼ 133.26; df ¼ 12 ; p , .0001; visual span forward: x2 ¼ 81.28; df ¼ 20; p , .0001; visual span, backward: x2 ¼ 133.26; df ¼ 12; p , .0001). However, performance did not improve at the same time for digit and visual spans. Digit spans mainly improved after the first training period (T1, addressing verbal working memory), then remained globally stable, except for a mild improvement of backward span after the third training stage (T3, addressing central executive functions). The highest span level successfully achieved at baseline was 4 both for forward and backward digit spans; it reached level 6 (forward) and 5 (backward) at T1 assessment, and then remained stable. In opposition, visual spans mainly improved after the second training stage (T2, addressing visuo-spatial working memory). The highest span level successfully achieved at baseline and at T1 was 6 for forward and 4 for backward visual spans; performance reached level 7 (forward) and 5 (backward) at T2 assessment. At the end of the trial, performance across the four different span measures (verbal and visual, forward and backward) was within the range of matched healthy controls. A visual presentation of performance on the two backward span measures is shown in the upper part of Figure 1. This figure illustrates the differential pattern of improvement with time for verbal and visual spans. On the Brown-Peterson task (Table 3) performance was poor and stable at Baseline, as compared to matched controls. AC showed great difficulty in recalling verbal or visual information, particularly after a 20-second delay, while simultaneously performing a concurrent task. Performance significantly improved after training (verbal task with articulatory suppression: x2 ¼ 33.82; df ¼ 8; p , .0001; verbal task with mental calculation: x2 ¼ 117.49 ; df ¼ 8 ; p , .0001; visual task with interference: x2 ¼ 34.84; df
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Figure 1. AC performance during the trial. The figures present the percentage of correct responses upon the two Baseline sessions (BL1 and BL2) and after each one of the three training phases (Post-T1, T2 and T3). Upper part: Digit and visual backward (B) spans. Lower part: BrownPeterson (BP) task; three conditions are represented: verbal BP with articulation and with mental calculation and visual BP with interfering task.
¼ 8; p , .0001). However, here again, improvement appeared related to the timing of intervention.
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The verbal Brown-Peterson task with articulatory suppression significantly improved after the first training stage. AC obtained only 10.6% hits at baseline, and reached nearly 80% hits after the first training stage. Afterwards, there was only a mild improvement. In contrast, the visual Brown-Peterson condition with interference improved mainly after the second training stage (10.6% hits at baseline, 22.6% at T1, and 72% at T2). The pattern of improvement was different however for the verbal Brown-Peterson task with mental calculation: Improvement occurred regularly for this task throughout the three training stages (starting from 27.3% hits at baseline to 88.6% at T3). Whatever the task condition, at the end of the trial the patient reached a performance within the range of matched healthy controls. A visual presentation of performance on the Brown-Peterson task is shown in the lower part of Figure 1, illustrating the differential pattern of improvement with time for verbal and visual Brown-Peterson tasks. Other central executive tasks included a 2-back and a divided attention task from the TAP (Zimmermann & Fimm, 2009). For practical reasons, these tasks were given only once before training. Performance (median Reaction Time) was compared to the published norms of the test battery (Zimmermann & Fimm, 2009) (mean standard score: 50, SD ¼ 10). Performance was below 1.6 SD of healthy controls before training (T ¼ 25 and T ¼ 34 for 2-back and divided attention subtest, respectively). It remained stable at T1 and T2 assessments (2-back: T ¼ 28; divided attention: T ¼ 31), and improved after the last training stage (2-back: T ¼ 45, divided attention, T ¼ 47). Non-specific tasks requiring working memory
Performance improved after the first training stage for verbal comprehension and the token test (going from 80% at baseline to 100% hits). Arithmetic problem solving improved from 66% hits at baseline to 83% at T1 and T2, and 100% at T3. There was a marginal improvement of mental flexibility at T3 (T ¼ 34 at baseline, T1 and T2, versus T ¼ 38 at T3). Ecological questionnaire. The Working Memory Questionnaire was given only once before starting training. The total score (out of 120, higher scores indicating more complaints) regularly decreased throughout the trial: Baseline ¼ 65, T1 ¼ 45, T2 ¼ 30, T3 ¼ 10. The T3 score fell within the range of healthy controls from the original validation study (n ¼ 313, mean total score ¼ 17.8, SD ¼ 11.5) (Vallat-Azouvi et al., 2012). Non-target tasks. There was a mild improvement after the first training stage of simple reaction time (T ¼ 55 on both baseline measures, T ¼ 66 at T1, T2 and T3), as well as of Complex Figure Recall (performance at
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the 50th percentile of healthy controls at baseline, and at the 90th percentile after training). There was no change of verbal learning as assessed with a word recognition task.
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DISCUSSION The objective of this single-case rehabilitation study was to assess the modularity of working memory training. In accordance with previous findings, the training as a whole was effective, as, at the end of the trial, AC’s performance on working memory measures had significantly improved and fell within the range of matched healthy controls. There was also a transfer to daily life. In addition, the results suggested some module-specific effects of training: indeed, verbal aspects of working memory (digit spans, both forward and backward, and the Brown-Peterson task with articulatory suppression) improved significantly after the first training stage focusing on the phonological loop. On the other hand, visuo-spatial aspects of working memory (visual spans, visual Brown-Peterson task with interference) improved mainly after the second training stage, focusing on visual and spatial working memory. Tests addressing central executive functions (i.e., requiring flexibility, updating, and/or task switching), such as n-back and divided attention tasks, improved mainly after the third training stage, focusing on executive aspects of working memory. Modularity effects were not as pronounced for other outcome measures, which seemed to improve throughout the trial, irrespective of the training condition: this was the case for the Brown-Peterson task with mental calculation. This latter task could be assumed to be less specific, and to tap all aspects of working memory, even though it requires the recall of verbal information. Similarly, the Working Memory Questionnaire, which addresses working memory in daily life, without disentangling verbal and visuospatial domains, also improved regularly during the trial. It is unlikely that these results were related to confounding effects, such as spontaneous recovery, retest or placebo effects. Indeed, the patient was at a chronic stage post-stroke (more than four years), at a time when spontaneous recovery is limited, and assessment was conducted blind from treatment assignment. To our knowledge, this is the first study showing such domain-specific effects in rehabilitation of working memory. Indeed, as mentioned in the Introduction section, most previous studies (with the exception of Duval et al., 2008, within a different theoretical framework) used a global training of the central executive, without trying to disentangle the training effects on the various subcomponents of working memory. These findings have both theoretical and clinical implications.
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From a theoretical point of view, the present results are in accordance with current psychological and neuroanatomical models of working memory. Such models assume that working memory relies both on modality-specific storage systems and on a multimodal control and coordination function (Baddeley, 2003; Engle, 2002). As a consequence, training focusing on verbal or visual storage might have relatively selective effects, while training focusing on multimodal (or amodal) controlling might have more widespread effects. This is what was found in the present study, and this may explain why the two first, modality-specific, training stages had only limited effects on central executive functions. However, the different subcomponents of working memory are not completely independent one from the other and some degree of transfer from one domain to the other was also found: for example, there was a mild improvement of forward visuo-spatial span and of the visual Brown-Peterson task after training of the phonological loop. Therefore, these findings support the modularity of working memory functions, but also underline the fact that the different subdomains within working memory are not completely independent from one another. There was also some mild improvement of untrained tasks requiring executive control (arithmetic problem solving, language comprehension, flexibility, complex figure recall), and of speed of processing. This is in accordance with previous findings suggesting that working memory training based on tasks requiring a high level of executive control (such as n-back or updating tasks) may induce improvement in performance in untrained tasks relying on executive functions and control of attention (Klingberg, 2010; Klingberg et al., 2005; Thorell, Lindqvist, Bergman Nutley, Bohlin, & Klingberg, 2009). These findings are also in accordance with current knowledge on the neural correlates of working memory. Functional neuro-imaging studies in healthy individuals showed that working memory functioning is related to the activation of distributed brain networks including both domain-specific and multimodal brain regions (Klingberg, 2010). Schematically, the activation of posterior sensory association cortices is dependent on the sensory modality of the stimuli, while the intraparietal and dorsolateral prefrontal cortices are activated by several modalities, and thus seem to reflect a multimodal control activity (Collette & van der Linden, 2002; Linden, 2007). As recently suggested by Klingberg (2010), training affecting modality-specific regions would not be expected to have transfer effects to other modalities, while training affecting higher association cortices could be expected to have more general effects. A few studies have investigated the effect of working memory training on brain activity, mainly in healthy individuals, but also in psychiatric patients. The results were somewhat difficult to interpret, as some studies reported increases (Olesen et al., 2004; Wexler, Anderson,
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Fulbright, & Gore, 2000) and another decreases (Dahlin, Neely, Larsson, Backman, & Nyberg, 2008) of activity in prefrontal and parietal areas. Further research is needed to provide a better knowledge of the neural bases of training of different subcomponents of working memory in patients with brain injury. From a clinical point of view, these findings suggest that rehabilitation should use a wide range of tasks, adapted to each individual patient’s impairments. Indeed, working memory deficits may differ from one patient to another, depending on the nature, size and localisation of the lesion. Some patients may be impaired more or less selectively on each one of the three main subcomponents. The present results suggest that, in such cases, training should focus selectively on the impaired component(s). In addition, the present findings may help to explain the negative results reported in a few studies that used only one type of training task (Redick et al., 2013). There are some limitations to the present study. Single-subject designs are often considered as less valid than group studies. However, many authors argued that single-case studies play an important role in evidence-based clinical practice of cognitive rehabilitation (Perdices & Tate, 2009; Wilson, 1987). Tate and colleagues (2008) proposed a rating scale to measure methodological quality of single-case experimental designs. The present study fulfils seven out of 10 criteria on this scale. The unmet criteria were the following: stability of baseline was established over two and not three occasions; continuous measures of behaviour were not taken during the treatment phase; and reliability data exist for some, but not all outcome measures. All other criteria were met. Another limitation comes from the fact that it was unfortunately not possible to complete a late follow-up assessment, so it is not possible to say whether improvement lasted over time. However, a previous case report using the same rehabilitation programme with late follow-up suggested that the beneficial effect of rehabilitation lasted at least three months (Vallat-Azouvi et al., 2009). Another limitation was that original neuro-imaging data were unfortunately not available, and the patient did not wish to come back for neuro-imaging. Nevertheless, data from acute medical charts indicated that AC suffered from a retrorolandic ischaemic stroke, which is in accordance with current knowledge on the role of parietal areas in working memory, as discussed above. In conclusion, this case study suggests that there are both domain-specific and generalisation effects in rehabilitation of working memory. Rehabilitation of patients with limitations of working memory should include different type of training tasks, individually adapted and tailored to each individual patient’s impairments.
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REFERENCES Baddeley, A. (2003). Working memory: Looking back and looking forward. [Review]. Nature reviews. Neuroscience, 4, 829– 839. Baddeley, A. D., Baddeley, H. A., Bucks, R. S., & Wilcock, G. K. (2001). Attentional control in Alzheimer’s disease. Brain, 124, 1492 – 1508. Collette, F., & van der Linden, M. (2002). Brain imaging of the central executive component of working memory. Neuroscience and Biobehavioral Reviews, 26, 105– 125. Couillet, J., Soury, S., Lebornec, G., Asloun, S., Joseph, P. A., Mazaux, J. M., & Azouvi, P. (2010). Rehabilitation of divided attention after severe traumatic brain injury: A randomised trial. Neuropsychological Rehabilitation, 20, 321 –339. Dahlin, E., Neely, A. S., Larsson, A., Backman, L., & Nyberg, L. (2008). Transfer of learning after updating training mediated by the striatum. Science, 320, 1510 –1512. Daneman, M., & Carpenter, P. (1980). Individual differences in working memory and reading. Journal of Verbal Learning and Verbal Behavior, 19, 450 – 466. De Renzi, E., & Vignolo, L. A. (1962). The token test: A sensitive test to detect receptive disturbances in aphasics. Brain, 85, 665 – 678. Deloche, G., Metz-Lutz, M. N., Kremin, H., Hannequin, D., Ferrand, I., Perrier, D., . . . Naud, E. (1997). Test de De´nomination Orale de 80 images: DO 80. Paris: Edition du Centre de Psychologie Applique´e. Deloche, G., Seron, X., Larroque, C., Magnien, C., Metz-Lutz, M. N., Noel, M. N., . . . Pradatdiehl, P. (1994). Calculation and number processing: Assessment battery; role of demographic factors. Journal of Clinical and Experimental Neuropsychology, 16, 195 – 208. Ducarne de Ribeaucourt, B. (1989). Examen de l’aphasie. Paris: Edition du Centre de Psychologie Applique´e. Duval, J., Coyette, F., & Seron, X. (2008). Rehabilitation of the central executive component of working memory: A re-organisation approach applied to a single case. Neuropsychological Rehabilitation, 18, 430 – 460. Engle, R. W. (2002). Working memory capacity as executive attention. Current Directions in Psychological Science, 11, 19 – 23. Holmes, J., Gathercole, S. E., & Dunning, D. L. (2009). Adaptive training leads to sustained enhancement of poor working memory in children. Developmental Science, 12, F9– 15. Jaeggi, S. M., Buschkuehl, M., Jonides, J., & Perrig, W. J. (2008). Improving fluid intelligence with training on working memory. Proceedings of the National Academy of Science of the U S A, 105, 6829 – 6833. Klingberg, T. (2010). Training and plasticity of working memory. Trends in Cognitive Science, 14, 317– 324. Klingberg, T., Fernell, E., Olesen, P. J., Johnson, M., Gustafsson, P., Dahlstrom, K., . . . Westerberg, H. (2005). Computerized training of working memory in children with ADHD – a randomized, controlled trial. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 177– 186. Klingberg, T., Forssberg, H., & Westerberg, H. (2002). Training of working memory in children with ADHD. Journal of Clinical and Experimental Neuropsychology, 24, 781 – 791. Linden, D. E. (2007). The working memory networks of the human brain. The Neuroscientist, 13, 257– 267. Lundqvist, A., Grundstrom, K., Samuelsson, K., & Ronnberg, J. (2010). Computerized training of working memory in a group of patients suffering from acquired brain injury. Brain injury, 24(10), 1173 – 1183. Martinussen, R., Hayden, J., Hogg-Johnson, S., & Tannock, R. (2005). A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 377– 384.
Downloaded by [University College London] at 11:58 12 November 2014
MODULARITY IN REHABILITATION OF WORKING MEMORY
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Montgomery, S. A., & Asberg, M. (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry, 134, 382– 389. Nespoulous., J. L., & Roch-Lecour, A. (1992). MT 86 – Protocole Montre´al-Toulouse d’examen linguistique de l’aphasie. Isbergues, France: Ortho-Edition. Olesen, P. J., Westerberg, H., & Klingberg, T. (2004). Increased prefrontal and parietal activity after training of working memory. Nature Neuroscience, 7, 75 – 79. Osterrieth, P. A. (1944). Le test de copie d’une figure complexe. Archives de Psychologie, 30, 206 – 356. Perdices, M., & Tate, R. L. (2009). Single-subject designs as a tool for evidence-based clinical practice: Are they unrecognised and undervalued? Neuropsychological Rehabilitation, 19, 904 – 927. Redick, T. S., Shipstead, Z., Harrison, T. L., Hicks, K. L., Fried, D. E., Hambrick, D. Z., . . . Engle, R. W. (2013). No evidence of intelligence improvement after working memory training: A randomized, placebo-controlled study. Journal of Experimental Psychology General, 142, 359 – 379. Rey, A. (1959). Test de copie et de reproduction de me´moire de figures ge´ome´triques complexes. Paris: Les Edition du Centre de Psychologie Applique´e. Rey, A. (1964). Examen clinique en neuropsychologie. Paris: Presse Universitaire de France. Serino, A., Ciaramelli, E., Santantonio, A. D., Malagu, S., Servadei, F., & Ladavas, E. (2007). A pilot study for rehabilitation of central executive deficits after traumatic brain injury. Brain Injury, 21, 11 –19. Tate, R. L., McDonald, S., Perdices, M., Togher, L., Schultz, R., & Savage, S. (2008). Rating the methodological quality of single-subject designs and n-of-1 trials: Introducing the Single-Case Experimental Design (SCED) Scale. Neuropsychological Rehabilitation, 18, 385 – 401. Thorell, L. B., Lindqvist, S., Bergman Nutley, S., Bohlin, G., & Klingberg, T. (2009). Training and transfer effects of executive functions in preschool children. Developmental Science, 12, 106 – 113. Vallat, C., Azouvi, P., Hardisson, H., Meffert, R., Tessier, C., & Pradat-Diehl, P. (2005). Rehabilitation of verbal working memory after left hemisphere stroke. Brain Injury, 19, 1157–1164. Vallat-Azouvi, C., Pradat-Diehl, P., & Azouvi, P. (2009). Rehabilitation of the central executive of working memory after severe traumatic brain injury: Two single-case studies. Brain Injury, 23, 585– 594. Vallat-Azouvi, C., Pradat-Diehl, P., & Azouvi, P. (2012). The Working Memory Questionnaire: A scale to assess everyday life problems related to deficits of working memory in brain injured patients. Neuropsychological Rehabilitation, 22, 634– 649. Vallat-Azouvi, C., Weber, T., Legrand, L., & Azouvi, P. (2007). Working memory after severe traumatic brain injury. Journal of the International Neuropsychological Society, 13, 770 – 780. Wechsler, D. (1991). WMS-R. Echelle clinique de me´moire de Wechsler-re´vise´e. Paris: Les Editions du Centre de Psychologie Applique´e. Westerberg, H., Jacobaeus, H., Hirvikoski, T., Clevberger, P., Ostensson, M. L., Bartfai, A., & Klingberg, T. (2007). Computerized working memory training after stroke – a pilot study. Brain Injury, 21, 21– 29. Westerberg, H., & Klingberg, T. (2007). Changes in cortical activity after training of working memory – a single-subject analysis. Physiology & Behavior, 92, 186 – 192. Wexler, B. E., Anderson, M., Fulbright, R. K., & Gore, J. C. (2000). Preliminary evidence of improved verbal working memory performance and normalization of task-related frontal lobe activation in schizophrenia following cognitive exercises. American Journal of Psychiatry, 157, 1694 – 1697.
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Downloaded by [University College London] at 11:58 12 November 2014
Wilson, B. A. (1987). Single-case experimental designs in neuropsychological rehabilitation. Journal of Clinical and Experimental Neuropsychology, 9, 527 – 544. Wright, H. H., & Shisler, R. J. (2005). Working memory in aphasia: Theory, measures, and clinical implications. American Journal of Speech-Language Pathology/American Speech-Language-Hearing Association, 14, 107 – 118. Zimmermann, P., & Fimm, B. (2002). A test battery for attentional performance. In M. Leclercq & P. Zimmermann (Eds.), Applied neuropsychology of attention (pp. 110 – 151). London: Psychology Press. Zimmermann, P., & Fimm, B. (2009). TAP: Tests d’e´valuation de l’attention, version 2.2. Adaptation Franc¸aise M. Leclercq. Herzogenrath, Germany: Vera Fimm, Psychologische Testsysteme.
APPENDIX TRAINING TASKS USED FOR REHABILITATION Verbal tasks (Vallat et al., 2005) . .
. . . .
. .
Reconstitution of words from oral spelling: The patient had to reconstruct and pronounce a word that was spelled out by the therapist. Reconstitution of words from oral spelling with a letter omitted: This is the same task as the previous one, but with a letter omitted, replaced by a "bip". Oral spelling. Odd or even number of letters in a word: The task was to find whether the number of letters in a word heard was odd or even. Reconstitution of words from syllables: The therapist presented cluttered syllable words that the subject had to reorder and pronounce. Alphabetic way: The therapist presented a letter and a calculation (addition or subtraction), and the patient had to find the target letter following the increasing or decreasing alphabetical order (for example, B + 6 ¼ H; E – 2 ¼ C). Word sorting in alphabetic order: The patient was required to sort a series of concrete words into alphabetic order. Acronyms: The task was to find out the word made from the initial phonemes of a list of words.
Visuo-spatial tasks (Vallat-Azouvi et al., 2009) . .
2-D mental imagery on a chessboard: The task required patients to move mentally from one position to another on an imagined chessboard. 2-D mental imagery on a calculator keyboard: The task required patients to move mentally from one key to another on an imagined calculator keyboard.
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3-D mental imagery: The task required patients to move mentally from one position to another on an imagined cube. Visual n-back: Three types of stimuli were used: playing cards; figures; geometrical forms. Patients were asked to say whether or not an item matched the item presented 1-, 2- or 3-back in the sequence.
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More demanding executive tasks .
.
.
N-back task-words: This was based on a word semantic categorisation task: series of 20 words were spoken out successively by the therapist, and the patient was asked to respond “yes” when a word was in the same semantic category as the target. Twelve difficulty levels were used, by varying working memory load (1- vs. 2-back), presentation rate (every 1 or 3 seconds), and word length (1, 2 or 3 syllables). N-back task-questions: A series of simple questions was presented verbally by the therapist (such as: “What is the name of the main river in Paris?”). The patient had to give the answer to the question presented one, two or three back in the series depending on the difficulty level. Task difficulty level was also manipulated by varying the presentation rate (every 10 or 5 seconds). If the patient did not know the answer, he was asked to repeat the question. Five series of questions were given per training session. Reading span task: This task was based on Daneman and Carpenter’s (1980) procedure: the patient was asked to read aloud series of sentences and to repeat afterwards the last word of each sentence, in the correct order. Eighteen difficulty levels were used, depending on the number of sentences, but also on sentence length, sentence syntactic complexity, last word length, and word concreteness and imageability.
Neuropsychological Rehabilitation: An International Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/pnrh20
Modularity in rehabilitation of working memory: A single-case study ab
bc
Claire Vallat-Azouvi , Pascale Pradat-Diehl
&
bde
Philippe Azouvi a
UGECAM-antenne UEROS-SAMSAH 92, Raymond Poincare hospital, Garches, France b
ER 6, UMPC, Paris, France
c
AP-HP, Salpétrière hospital, Department of Physical Medicine and Rehabilitation, Paris, France d
AP-HP, Raymond Poincare hospital, Department of Physical Medicine and Rehabilitation, Garches, France e
EA 4047, University of Versailles-Saint Quentin, France Published online: 19 Feb 2014.
To cite this article: Claire Vallat-Azouvi, Pascale Pradat-Diehl & Philippe Azouvi (2014) Modularity in rehabilitation of working memory: A single-case study, Neuropsychological Rehabilitation: An International Journal, 24:2, 220-237, DOI: 10.1080/09602011.2014.881294 To link to this article: http://dx.doi.org/10.1080/09602011.2014.881294
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Neuropsychological Rehabilitation, 2014 Vol. 24, No. 2, 220– 237, http://dx.doi.org/10.1080/09602011.2014.881294
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Modularity in rehabilitation of working memory: A single-case study Claire Vallat-Azouvi1,2, Pascale Pradat-Diehl2,3, and Philippe Azouvi2,4,5 1
UGECAM-antenne UEROS-SAMSAH 92, Raymond Poincare hospital, Garches, France 2 ER 6, UMPC, Paris, France 3 AP-HP, Salpe´trie`re hospital, Department of Physical Medicine and Rehabilitation, Paris, France 4 AP-HP, Raymond Poincare hospital, Department of Physical Medicine and Rehabilitation, Garches, France 5 EA 4047, University of Versailles-Saint Quentin, France (Received 13 June 2013; accepted 13 January 2014)
The objective of the present study was to assess the specificity of rehabilitation on different subdomains of working memory. A 38-year-old female with chronic (4 years) stroke suffered from an impairment of the three subdomains of working memory (modality-specific storage systems for verbal and visuo-spatial information and the central executive). She was given an experimental rehabilitation programme, using a multiple-baseline across behaviour design. After two baseline measures three months apart, the first training stage focused on the phonological loop, the second on the visuo-spatial sketchpad, and the third on central executive functions. Verbal aspects of working memory improved significantly after the first training stage, while visuo-spatial tests improved after the second training stage. Central executive functions improved mainly after the third training stage. Modularity effects were not as pronounced for less specific ecological outcome measures, such as the Working Memory Questionnaire, which improved throughout the trial, irrespective of the training condition. This case study suggests that there are both domain-specific and generalisation effects in rehabilitation of working memory, and that rehabilitation should be adapted and tailored to each individual patient’s impairments. Correspondence should be addressed to Claire Vallat-Azouvi, PhD, Antenne UEROSSAMSAH 92-UGECAM, Hoˆpital Raymond Poincare´, 92380 Garches, France. E-mail: claire. [email protected] # 2014 Taylor & Francis
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Keywords: Working memory; Rehabilitation; Stroke; Modularity; Cognition.
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INTRODUCTION Working memory is a complex system involved in short-term storage and simultaneous processing of information (Baddeley, 2003). This function, which is of great importance in many cognitive tasks, may be impaired in several neurological conditions, such as stroke (Wright & Shisler, 2005), traumatic brain injury (Vallat-Azouvi, Weber, Legrand, & Azouvi, 2007), Alzheimer’s disease (Baddeley, Baddeley, Bucks, & Wilcock, 2001), or in children with attention deficit hyperactivity disorder (ADHD) (Martinussen, Hayden, Hogg-Johnson, & Tannock, 2005). Current theoretical and neuro-anatomical models of working memory suggest that it relies on at least two distinct modality-specific storage systems, and on a multimodal controlling function. The modality-specific storage systems are usually referred to as the phonological loop (for verbal information) and the visuo-spatial sketchpad (for visual and spatial information), while the multimodal controlling and coordinating system has been called the central executive, or controlled or executive attention (Baddeley, 2003; Engle, 2002). Recent group and single-case studies suggest that intensive training may improve working memory in patients suffering from stroke (Lundqvist, Grundstrom, Samuelsson, & Ronnberg, 2010; Vallat et al., 2005; Westerberg et al., 2007), traumatic brain injury (Couillet et al., 2010; Serino et al., 2007; Vallat-Azouvi, Pradat-Diehl, & Azouvi, 2009), brain tumour (Duval, Coyette, & Seron, 2008), and in children with ADHD (Holmes, Gathercole, & Dunning, 2009; Klingberg et al., 2005; Klingberg, Forssberg, & Westerberg, 2002; Martinussen et al., 2005). Adapted and extended training has also been found to enhance working memory capacity in healthy individuals, associated with changes in brain activity in frontal and parietal cortex and basal ganglia (Jaeggi, Buschkuehl, Jonides, & Perrig, 2008; Olesen, Westerberg, & Klingberg, 2004; Westerberg & Klingberg, 2007), although conflicting results have been reported (Redick et al., 2013) (for a recent review see Klingberg, 2010). However, most studies used either one single training task, or a combination of tasks given to all patients in a similar way. To our knowledge, there has not been any attempt to disentangle the effect of training on the various subcomponents of working memory. The only exception was the study by Duval et al. (2008), but these authors used a different theoretical framework, and trained successively the following three sub-components of the central executive: processing load, updating and dual-task monitoring. The programme proved to be effective for all three working memory components, but the specificity of training was limited.
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The issue of specificity of training is important in two aspects. First, from a theoretical point of view, if training effects are domain-specific, this supports the idea that working memory components may be modular and independent in terms of processing requirements (and eventually neuroanatomical location). On the other hand, if generalisation takes place this is most probably not the case and the components of working memory might share these requirements. Second, from a clinical point of view, all patients do not show the same pattern of impairment, and it could be assumed that training should be adapted to the specific impairment of an individual patient. We present a single-case rehabilitation study of a patient with chronic left hemisphere stroke suffering from a selective impairment of working memory involving the three domains (the phonological loop, the visuo-spatial sketchpad and the central executive). Training was given in three stages, focusing successively on each one of these three domains, in order to assess the domain-specific and the generalisation effects of training within working memory.
CASE REPORT AC was a 38-year-old woman, working as assistant manager in a bank, who suffered from an ischaemic stroke in the retrorolandic part of the superficial left sylvian arterial territory. At the acute stage, she presented a severe aphasia, with mutism and bucco-facial apraxia, but preserved comprehension, except for long sentences and for written texts. Her condition improved progressively and when she was referred to our rehabilitation department, a few weeks after stroke, her language impairment was considered as characteristic of a conduction aphasia. After a few months of speech and language therapy, her language showed a very good recovery. However, despite this dramatic improvement of language abilities, she still continued to complain of difficulty in dual-task situations, and also in taking notes, concentrating, memorising information in the short-term, holding a conversation, and of mental fatigue. A comprehensive neuropsychological assessment was carried out four years and three months post stroke onset (Table 1). At this time, language, as assessed with conventional aphasia tests, had nearly fully recovered, as shown by scores at ceiling on naming, picture description, written comprehension, and syntactic comprehension tests. Long-term verbal episodic memory, reasoning, planning, flexibility and basic attentional abilities were preserved, with the exception of a moderate slowing in choice reaction time tasks. There was no sign of anxiety or depression, and the patient scored below cut-off on a depression scale. There was however a mild impairment of written text comprehension, and of both arithmetical and logical problem solving. Her verbal span was 4
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TABLE 1 First baseline neuropsychological assessment
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Tasks Language Naming (DO80)a Figure description b Syntactic oral comprehension b,c Oral comprehension (% hits) b,c Token Test (written form) d Token Test (oral form) d Written text comprehension (MT86) c Written syntactic comprehension (Rey’s 15 questions)e Calculation (EC301) f Attention (TAP)g Phasic alertness, median RT (Standard score) Flexibility, median RT (Standard score) Flexibility, errors (Standard score) Selective attention, median RT (Standard score) Selective attention, errors (Standard score) Episodic memory Complex figure recall (centile) h Word list learning (Rey, Centile) e Paired associate learning (WMS-R) i Problem solving Arithmetic problem solving (% hits) b Logic verbal problem solving b Working memory j Digit span, forward Digit span, backward Visual span, forward Visual span, backward Depression (MADRS) k
AC score/maximal score
80/80 18/18 38/38 80 36/36 29/36 6/6 15/15 92/92 55 34 46 20 44 50 75 24/24 66 4,5/6 4 4 6 4 6/60
a DO80: naming test (Deloche et al., 1997); b,caphasia batteries (Ducarne de Ribeaucourt, 1989; Nespoulous. & Roch-Lecour, 1992); dToken Test (De Renzi & Vignolo, 1962); eAuditory Verbal Learning Test (Rey, 1964); fcalculation assessment (Deloche et al., 1994) ;gTAP (Zimmermann & Fimm, 2002) (mean standard note ¼ 50, SD ¼ 10); hComplex Figure (Osterrieth, 1944); iWechsler Memory Scale–Revised (Wechsler, 1991); jWorking Memory Assessment (Vallat-Azouvi et al., ˚ sberg Depression Rating Scale (MADRS; Montgomery & Asberg, 1979). 2007); kMontgomery–A
(both forward and backward), and forward and backward visuo-spatial spans were 6 and 4, respectively, thus suggesting a working memory deficit. A more detailed assessment focusing on working memory was then given, which revealed an isolated and severe deficit of all components of working memory, including the phonological loop, the visuo-spatial sketchpad and the central executive. Central executive tasks, such as the Brown-Peterson tasks of short-term memory with interference were significantly impaired,
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in comparison with matched controls, both in the verbal and visual modalities (she was unable to maintain three items in short-term memory for 20 seconds, while simultaneously performing a resource demanding task). Detailed performance on working memory tasks will be presented later (see Results section and Tables 2 and 3). It was then decided to propose to AC a specific training of working memory, following a previously described methodology (Vallat et al., 2005; VallatAzouvi et al., 2009). However, in order to disentangle the effects of rehabilitation on the different subcomponents of working memory, training focusing on the phonological loop, the visuo-spatial sketchpad and the central executive was given separately and successively. The patient was informed of the experimental aim of the study and gave her consent to participate. Data were obtained in compliance with the Helsinki Declaration.
Experimental design A single-case multiple baseline-across behaviours design was used (Wilson, 1987). Three successive training stages were proposed. The first stage focused on training of the phonological loop, the second stage on the visuo-spatial sketchpad, and the third stage on the central executive. Although AC was at a chronic stage, to control for re-test effects, and to produce a more reliable baseline assessment, two baseline measures of different components of working memory were taken before starting training (BL1 and BL2), with a three month inter-test interval. Outcome measures were obtained just after the end of each training stage (they will be referred to as T1, T2 and T3, respectively).
Training The training tasks used in the two first stages have been described in detail in two previous papers (Vallat et al., 2005; Vallat-Azouvi et al., 2009). Training addressed both storage and processing of information in working memory. Eight tasks addressing verbal aspects of working memory were used in the first training stage (reconstitution of words from oral spelling, with or without a letter omitted, oral spelling, odd or even number of letters in a word, reconstitution of words from syllables, alphabetic way, word sorting in alphabetic order, acronyms). Four tasks addressing the visuo-spatial sketchpad were used in the second training stage (2-D mental imagery on a chessboard, 2-D mental imagery on a calculator keyboard, 3-D mental imagery, visual n-back). A description of these 12 tasks can be found in the Appendix at the end of this paper. In the last stage, focusing on central executive functions, new tasks were designed in order to tap more intensively executive aspects of working memory. These tasks (also presented in more detail in the Appendix) required simultaneous storage and processing of
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TABLE 2 Performance on PM tasks and measures of neuropsychological functioning Digit span, forward
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Controls BL1 BL2 Post-T1 Post-T2 Post-T3 Digit span, backward Controls BL1 BL2 Post-T1 Post-T2 Post-T3 Visual span, forward Controls BL1 BL2 Post-T1 Post-T2 Post-T3 Visual span, backward Controls BL1 BL2 Post-T1 Post-T2 Post-T3
2
3
100 (0.00) 100 (0.00)
4 100 (0.00)
5
6
83.27 (29.01) 63.33 (39.79)
100 100 100 100 100
80 60 100 100 100
60 60 100 100 100
0 0 100 100 100
0 0 40 40 40
2
3
4
5
6
100 (0.00) 100 (0.00) 89.87 (15.17) 66.66 (45.65) 46.66 (43.14) 100 100 100 100 100
80 60 100 100 100
40 40 100 100 100
2
3
4
100 (0.00) 100 (0.00) 96.67 (7.46)
0 0 40 40 80 5 70 (36.13)
0 0 0 0 0 6
100 80 100 100 100
80 80 100 100 100
60 60 100 100 100
40 40 80 100 100
60 40 80 100 100
2
3
4
5
6
100 (0.00) 100 (0.00) 93.33 (9.13) 100 100 100 100 100
80 60 80 100 100
40 40 40 100 100
70 (32.06) 0 0 0 40 80
7
13.33 (18.26) 3.33 (7.45) 0 0 0 20 20
16.66 (20.41) 0 0 0 0 0
BL ¼ baseline; Post-T1, T2 and T3 refer to the three post-training outcome measures.
information: n-back tasks using words or questions, and reading span tasks were used (Daneman & Carpenter, 1980). The tasks were arranged in a difficulty hierarchy order organised to follow two criteria, capacity (amount of information) and level of processing (stimulus complexity). Training was given during two one-hour sessions per week. Training stages 1 and 2 lasted six months each, and training stage 3 lasted seven months. The difficulty level was progressively adapted to the patient’s
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VALLAT-AZOUVI, PRADAT-DIEHL, AND AZOUVI TABLE 3 Verbal and visual Brown-Peterson (BP) tasks). Recall delay (sec) 5
10
100 (0.00)
100 (0.00)
BL1 BL2
16 16
16 16
0 0
Post-T1 Post-T2 Post-T3
66 83 100
83 83 100
83 83 83
5
10
20
96 (8.94)
96 (8.94)
BL1 BL2
66 66
16 16
0 0
Post-T1 Post-T2 Post-T3
33 83 100
33 50 83
50 50 83
5
10
20
100 (0.00)
96.67 (7.46)
BL1 BL2
16 16
16 16
0 0
Post-T1 Post-T2 Post-T3
33 83 83
16 83 100
16 50 83
BP- articulatory suppression
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Controls
BP-mental calculation Controls
Visual BP-with interference Controls
20 100 (0.00)
80 (24.49)
100 (0.00)
BL ¼ baseline; Post-T1, T2 and T3 refer to the three post-training outcome measures.
performance, starting at the n-1 backward digit span level. Each level was trained until the patient succeeded in 90% of the trials.
Outcome measures Four sets of outcome measures were used, including non-target measures to assess the specificity of training (see Vallat-Azouvi et al., 2009, for a more detailed presentation of the tasks). Cognitive tasks specifically designed to assess the different components of working memory. The phonological loop and the visuo-spatial sketchpad were assessed with forward and backward digit and visuo-spatial spans, respectively (five trials for each span length). The central executive was
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assessed with the Brown-Peterson paradigm, both in the verbal and visual modalities. This task requires recalling short pieces of verbal or visual information after a delay of 5, 10 or 20 seconds, while simultaneously performing a concurrent distracting task of increasing complexity. Central executive functions were additionally assessed with the 2-back and the divided attention subtasks of the Test for Attentional Performance (TAP; Zimmermann & Fimm, 2009). Non-specific tasks requiring working memory. These included tasks that were not specifically designed to assess working memory, that were not trained, but that nevertheless include a high working memory load. This subset of tasks included arithmetic problem solving (15 problems of increasing complexity), sentence comprehension (Ducarne de Ribeaucourt, 1989), the Token test (De Renzi & Vignolo, 1962), and the mental flexibility subtest of the TAP (Zimmermann & Fimm, 2009). Ecological questionnaire. The Working Memory Questionnaire (WMQ; Vallat-Azouvi, Pradat-Diehl, & Azouvi, 2012) has been designed specifically to assess everyday life difficulties related to working memory failures. It is a self-assessment questionnaire comprising 30 questions scored on a five-point Likert scale, ranging from 0 (“no problem at all”) to 4 (“very severe problem in everyday life”). It has been previously found sensitive to brain damage (Vallat-Azouvi et al., 2012). Non-target tasks. These measures were assumed not to require working memory, and were not expected to improve after therapy. Non-target measures included the following: a simple visual reaction time, from the TAP; two long-term verbal memory tasks: a word recognition task in which 30 words were presented orally to the patients, and had to be recognised 20 minutes later, mixed with 60 distractors; and a test of visual longterm memory, Complex Figure Recall (Rey, 1959). To control for re-test effects, parallel versions of the tasks were designed and outcome measures were always different from the tasks used for the therapy. To reduce as far as possible an examiner’s bias, therapy and assessment were performed by different investigators, blind one from each other. Data have been analysed by comparison of AC’s performance to that of five healthy subjects matched for age and education (three men, mean age ¼ 40 +/- 1.87 years, mean education duration ¼ 12 +/2.5 years), with the exception of outcome measures from the TAP, which were compared to the published norms for this battery (Zimmermann & Fimm, 2009).
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Data analysis
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For the main outcome measures (spans and Brown-Peterson tasks), statistical analyses were computed using Chi-2 statistics on the percentage of correct responses on the five successive testing sessions. Such analysis could not be conducted on other measures, for which data analysis relied on comparison of AC’s mean standardised scores to published norms for the tests, when available, or on visual inspection of data when norms were not available.
Results The results of cognitive tasks specifically designed to assess the different components of working memory are presented in Tables 2 and 3. Performance was stable on the two baseline measures of digit and visual spans (Table 2) and significantly improved after therapy (digit span, forward: x2 ¼ 211.03; df ¼ 16; p , .0001; digit span, backward: x2 ¼ 133.26; df ¼ 12 ; p , .0001; visual span forward: x2 ¼ 81.28; df ¼ 20; p , .0001; visual span, backward: x2 ¼ 133.26; df ¼ 12; p , .0001). However, performance did not improve at the same time for digit and visual spans. Digit spans mainly improved after the first training period (T1, addressing verbal working memory), then remained globally stable, except for a mild improvement of backward span after the third training stage (T3, addressing central executive functions). The highest span level successfully achieved at baseline was 4 both for forward and backward digit spans; it reached level 6 (forward) and 5 (backward) at T1 assessment, and then remained stable. In opposition, visual spans mainly improved after the second training stage (T2, addressing visuo-spatial working memory). The highest span level successfully achieved at baseline and at T1 was 6 for forward and 4 for backward visual spans; performance reached level 7 (forward) and 5 (backward) at T2 assessment. At the end of the trial, performance across the four different span measures (verbal and visual, forward and backward) was within the range of matched healthy controls. A visual presentation of performance on the two backward span measures is shown in the upper part of Figure 1. This figure illustrates the differential pattern of improvement with time for verbal and visual spans. On the Brown-Peterson task (Table 3) performance was poor and stable at Baseline, as compared to matched controls. AC showed great difficulty in recalling verbal or visual information, particularly after a 20-second delay, while simultaneously performing a concurrent task. Performance significantly improved after training (verbal task with articulatory suppression: x2 ¼ 33.82; df ¼ 8; p , .0001; verbal task with mental calculation: x2 ¼ 117.49 ; df ¼ 8 ; p , .0001; visual task with interference: x2 ¼ 34.84; df
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Figure 1. AC performance during the trial. The figures present the percentage of correct responses upon the two Baseline sessions (BL1 and BL2) and after each one of the three training phases (Post-T1, T2 and T3). Upper part: Digit and visual backward (B) spans. Lower part: BrownPeterson (BP) task; three conditions are represented: verbal BP with articulation and with mental calculation and visual BP with interfering task.
¼ 8; p , .0001). However, here again, improvement appeared related to the timing of intervention.
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The verbal Brown-Peterson task with articulatory suppression significantly improved after the first training stage. AC obtained only 10.6% hits at baseline, and reached nearly 80% hits after the first training stage. Afterwards, there was only a mild improvement. In contrast, the visual Brown-Peterson condition with interference improved mainly after the second training stage (10.6% hits at baseline, 22.6% at T1, and 72% at T2). The pattern of improvement was different however for the verbal Brown-Peterson task with mental calculation: Improvement occurred regularly for this task throughout the three training stages (starting from 27.3% hits at baseline to 88.6% at T3). Whatever the task condition, at the end of the trial the patient reached a performance within the range of matched healthy controls. A visual presentation of performance on the Brown-Peterson task is shown in the lower part of Figure 1, illustrating the differential pattern of improvement with time for verbal and visual Brown-Peterson tasks. Other central executive tasks included a 2-back and a divided attention task from the TAP (Zimmermann & Fimm, 2009). For practical reasons, these tasks were given only once before training. Performance (median Reaction Time) was compared to the published norms of the test battery (Zimmermann & Fimm, 2009) (mean standard score: 50, SD ¼ 10). Performance was below 1.6 SD of healthy controls before training (T ¼ 25 and T ¼ 34 for 2-back and divided attention subtest, respectively). It remained stable at T1 and T2 assessments (2-back: T ¼ 28; divided attention: T ¼ 31), and improved after the last training stage (2-back: T ¼ 45, divided attention, T ¼ 47). Non-specific tasks requiring working memory
Performance improved after the first training stage for verbal comprehension and the token test (going from 80% at baseline to 100% hits). Arithmetic problem solving improved from 66% hits at baseline to 83% at T1 and T2, and 100% at T3. There was a marginal improvement of mental flexibility at T3 (T ¼ 34 at baseline, T1 and T2, versus T ¼ 38 at T3). Ecological questionnaire. The Working Memory Questionnaire was given only once before starting training. The total score (out of 120, higher scores indicating more complaints) regularly decreased throughout the trial: Baseline ¼ 65, T1 ¼ 45, T2 ¼ 30, T3 ¼ 10. The T3 score fell within the range of healthy controls from the original validation study (n ¼ 313, mean total score ¼ 17.8, SD ¼ 11.5) (Vallat-Azouvi et al., 2012). Non-target tasks. There was a mild improvement after the first training stage of simple reaction time (T ¼ 55 on both baseline measures, T ¼ 66 at T1, T2 and T3), as well as of Complex Figure Recall (performance at
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the 50th percentile of healthy controls at baseline, and at the 90th percentile after training). There was no change of verbal learning as assessed with a word recognition task.
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DISCUSSION The objective of this single-case rehabilitation study was to assess the modularity of working memory training. In accordance with previous findings, the training as a whole was effective, as, at the end of the trial, AC’s performance on working memory measures had significantly improved and fell within the range of matched healthy controls. There was also a transfer to daily life. In addition, the results suggested some module-specific effects of training: indeed, verbal aspects of working memory (digit spans, both forward and backward, and the Brown-Peterson task with articulatory suppression) improved significantly after the first training stage focusing on the phonological loop. On the other hand, visuo-spatial aspects of working memory (visual spans, visual Brown-Peterson task with interference) improved mainly after the second training stage, focusing on visual and spatial working memory. Tests addressing central executive functions (i.e., requiring flexibility, updating, and/or task switching), such as n-back and divided attention tasks, improved mainly after the third training stage, focusing on executive aspects of working memory. Modularity effects were not as pronounced for other outcome measures, which seemed to improve throughout the trial, irrespective of the training condition: this was the case for the Brown-Peterson task with mental calculation. This latter task could be assumed to be less specific, and to tap all aspects of working memory, even though it requires the recall of verbal information. Similarly, the Working Memory Questionnaire, which addresses working memory in daily life, without disentangling verbal and visuospatial domains, also improved regularly during the trial. It is unlikely that these results were related to confounding effects, such as spontaneous recovery, retest or placebo effects. Indeed, the patient was at a chronic stage post-stroke (more than four years), at a time when spontaneous recovery is limited, and assessment was conducted blind from treatment assignment. To our knowledge, this is the first study showing such domain-specific effects in rehabilitation of working memory. Indeed, as mentioned in the Introduction section, most previous studies (with the exception of Duval et al., 2008, within a different theoretical framework) used a global training of the central executive, without trying to disentangle the training effects on the various subcomponents of working memory. These findings have both theoretical and clinical implications.
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From a theoretical point of view, the present results are in accordance with current psychological and neuroanatomical models of working memory. Such models assume that working memory relies both on modality-specific storage systems and on a multimodal control and coordination function (Baddeley, 2003; Engle, 2002). As a consequence, training focusing on verbal or visual storage might have relatively selective effects, while training focusing on multimodal (or amodal) controlling might have more widespread effects. This is what was found in the present study, and this may explain why the two first, modality-specific, training stages had only limited effects on central executive functions. However, the different subcomponents of working memory are not completely independent one from the other and some degree of transfer from one domain to the other was also found: for example, there was a mild improvement of forward visuo-spatial span and of the visual Brown-Peterson task after training of the phonological loop. Therefore, these findings support the modularity of working memory functions, but also underline the fact that the different subdomains within working memory are not completely independent from one another. There was also some mild improvement of untrained tasks requiring executive control (arithmetic problem solving, language comprehension, flexibility, complex figure recall), and of speed of processing. This is in accordance with previous findings suggesting that working memory training based on tasks requiring a high level of executive control (such as n-back or updating tasks) may induce improvement in performance in untrained tasks relying on executive functions and control of attention (Klingberg, 2010; Klingberg et al., 2005; Thorell, Lindqvist, Bergman Nutley, Bohlin, & Klingberg, 2009). These findings are also in accordance with current knowledge on the neural correlates of working memory. Functional neuro-imaging studies in healthy individuals showed that working memory functioning is related to the activation of distributed brain networks including both domain-specific and multimodal brain regions (Klingberg, 2010). Schematically, the activation of posterior sensory association cortices is dependent on the sensory modality of the stimuli, while the intraparietal and dorsolateral prefrontal cortices are activated by several modalities, and thus seem to reflect a multimodal control activity (Collette & van der Linden, 2002; Linden, 2007). As recently suggested by Klingberg (2010), training affecting modality-specific regions would not be expected to have transfer effects to other modalities, while training affecting higher association cortices could be expected to have more general effects. A few studies have investigated the effect of working memory training on brain activity, mainly in healthy individuals, but also in psychiatric patients. The results were somewhat difficult to interpret, as some studies reported increases (Olesen et al., 2004; Wexler, Anderson,
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Fulbright, & Gore, 2000) and another decreases (Dahlin, Neely, Larsson, Backman, & Nyberg, 2008) of activity in prefrontal and parietal areas. Further research is needed to provide a better knowledge of the neural bases of training of different subcomponents of working memory in patients with brain injury. From a clinical point of view, these findings suggest that rehabilitation should use a wide range of tasks, adapted to each individual patient’s impairments. Indeed, working memory deficits may differ from one patient to another, depending on the nature, size and localisation of the lesion. Some patients may be impaired more or less selectively on each one of the three main subcomponents. The present results suggest that, in such cases, training should focus selectively on the impaired component(s). In addition, the present findings may help to explain the negative results reported in a few studies that used only one type of training task (Redick et al., 2013). There are some limitations to the present study. Single-subject designs are often considered as less valid than group studies. However, many authors argued that single-case studies play an important role in evidence-based clinical practice of cognitive rehabilitation (Perdices & Tate, 2009; Wilson, 1987). Tate and colleagues (2008) proposed a rating scale to measure methodological quality of single-case experimental designs. The present study fulfils seven out of 10 criteria on this scale. The unmet criteria were the following: stability of baseline was established over two and not three occasions; continuous measures of behaviour were not taken during the treatment phase; and reliability data exist for some, but not all outcome measures. All other criteria were met. Another limitation comes from the fact that it was unfortunately not possible to complete a late follow-up assessment, so it is not possible to say whether improvement lasted over time. However, a previous case report using the same rehabilitation programme with late follow-up suggested that the beneficial effect of rehabilitation lasted at least three months (Vallat-Azouvi et al., 2009). Another limitation was that original neuro-imaging data were unfortunately not available, and the patient did not wish to come back for neuro-imaging. Nevertheless, data from acute medical charts indicated that AC suffered from a retrorolandic ischaemic stroke, which is in accordance with current knowledge on the role of parietal areas in working memory, as discussed above. In conclusion, this case study suggests that there are both domain-specific and generalisation effects in rehabilitation of working memory. Rehabilitation of patients with limitations of working memory should include different type of training tasks, individually adapted and tailored to each individual patient’s impairments.
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REFERENCES Baddeley, A. (2003). Working memory: Looking back and looking forward. [Review]. Nature reviews. Neuroscience, 4, 829– 839. Baddeley, A. D., Baddeley, H. A., Bucks, R. S., & Wilcock, G. K. (2001). Attentional control in Alzheimer’s disease. Brain, 124, 1492 – 1508. Collette, F., & van der Linden, M. (2002). Brain imaging of the central executive component of working memory. Neuroscience and Biobehavioral Reviews, 26, 105– 125. Couillet, J., Soury, S., Lebornec, G., Asloun, S., Joseph, P. A., Mazaux, J. M., & Azouvi, P. (2010). Rehabilitation of divided attention after severe traumatic brain injury: A randomised trial. Neuropsychological Rehabilitation, 20, 321 –339. Dahlin, E., Neely, A. S., Larsson, A., Backman, L., & Nyberg, L. (2008). Transfer of learning after updating training mediated by the striatum. Science, 320, 1510 –1512. Daneman, M., & Carpenter, P. (1980). Individual differences in working memory and reading. Journal of Verbal Learning and Verbal Behavior, 19, 450 – 466. De Renzi, E., & Vignolo, L. A. (1962). The token test: A sensitive test to detect receptive disturbances in aphasics. Brain, 85, 665 – 678. Deloche, G., Metz-Lutz, M. N., Kremin, H., Hannequin, D., Ferrand, I., Perrier, D., . . . Naud, E. (1997). Test de De´nomination Orale de 80 images: DO 80. Paris: Edition du Centre de Psychologie Applique´e. Deloche, G., Seron, X., Larroque, C., Magnien, C., Metz-Lutz, M. N., Noel, M. N., . . . Pradatdiehl, P. (1994). Calculation and number processing: Assessment battery; role of demographic factors. Journal of Clinical and Experimental Neuropsychology, 16, 195 – 208. Ducarne de Ribeaucourt, B. (1989). Examen de l’aphasie. Paris: Edition du Centre de Psychologie Applique´e. Duval, J., Coyette, F., & Seron, X. (2008). Rehabilitation of the central executive component of working memory: A re-organisation approach applied to a single case. Neuropsychological Rehabilitation, 18, 430 – 460. Engle, R. W. (2002). Working memory capacity as executive attention. Current Directions in Psychological Science, 11, 19 – 23. Holmes, J., Gathercole, S. E., & Dunning, D. L. (2009). Adaptive training leads to sustained enhancement of poor working memory in children. Developmental Science, 12, F9– 15. Jaeggi, S. M., Buschkuehl, M., Jonides, J., & Perrig, W. J. (2008). Improving fluid intelligence with training on working memory. Proceedings of the National Academy of Science of the U S A, 105, 6829 – 6833. Klingberg, T. (2010). Training and plasticity of working memory. Trends in Cognitive Science, 14, 317– 324. Klingberg, T., Fernell, E., Olesen, P. J., Johnson, M., Gustafsson, P., Dahlstrom, K., . . . Westerberg, H. (2005). Computerized training of working memory in children with ADHD – a randomized, controlled trial. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 177– 186. Klingberg, T., Forssberg, H., & Westerberg, H. (2002). Training of working memory in children with ADHD. Journal of Clinical and Experimental Neuropsychology, 24, 781 – 791. Linden, D. E. (2007). The working memory networks of the human brain. The Neuroscientist, 13, 257– 267. Lundqvist, A., Grundstrom, K., Samuelsson, K., & Ronnberg, J. (2010). Computerized training of working memory in a group of patients suffering from acquired brain injury. Brain injury, 24(10), 1173 – 1183. Martinussen, R., Hayden, J., Hogg-Johnson, S., & Tannock, R. (2005). A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 377– 384.
Downloaded by [University College London] at 11:58 12 November 2014
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Montgomery, S. A., & Asberg, M. (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry, 134, 382– 389. Nespoulous., J. L., & Roch-Lecour, A. (1992). MT 86 – Protocole Montre´al-Toulouse d’examen linguistique de l’aphasie. Isbergues, France: Ortho-Edition. Olesen, P. J., Westerberg, H., & Klingberg, T. (2004). Increased prefrontal and parietal activity after training of working memory. Nature Neuroscience, 7, 75 – 79. Osterrieth, P. A. (1944). Le test de copie d’une figure complexe. Archives de Psychologie, 30, 206 – 356. Perdices, M., & Tate, R. L. (2009). Single-subject designs as a tool for evidence-based clinical practice: Are they unrecognised and undervalued? Neuropsychological Rehabilitation, 19, 904 – 927. Redick, T. S., Shipstead, Z., Harrison, T. L., Hicks, K. L., Fried, D. E., Hambrick, D. Z., . . . Engle, R. W. (2013). No evidence of intelligence improvement after working memory training: A randomized, placebo-controlled study. Journal of Experimental Psychology General, 142, 359 – 379. Rey, A. (1959). Test de copie et de reproduction de me´moire de figures ge´ome´triques complexes. Paris: Les Edition du Centre de Psychologie Applique´e. Rey, A. (1964). Examen clinique en neuropsychologie. Paris: Presse Universitaire de France. Serino, A., Ciaramelli, E., Santantonio, A. D., Malagu, S., Servadei, F., & Ladavas, E. (2007). A pilot study for rehabilitation of central executive deficits after traumatic brain injury. Brain Injury, 21, 11 –19. Tate, R. L., McDonald, S., Perdices, M., Togher, L., Schultz, R., & Savage, S. (2008). Rating the methodological quality of single-subject designs and n-of-1 trials: Introducing the Single-Case Experimental Design (SCED) Scale. Neuropsychological Rehabilitation, 18, 385 – 401. Thorell, L. B., Lindqvist, S., Bergman Nutley, S., Bohlin, G., & Klingberg, T. (2009). Training and transfer effects of executive functions in preschool children. Developmental Science, 12, 106 – 113. Vallat, C., Azouvi, P., Hardisson, H., Meffert, R., Tessier, C., & Pradat-Diehl, P. (2005). Rehabilitation of verbal working memory after left hemisphere stroke. Brain Injury, 19, 1157–1164. Vallat-Azouvi, C., Pradat-Diehl, P., & Azouvi, P. (2009). Rehabilitation of the central executive of working memory after severe traumatic brain injury: Two single-case studies. Brain Injury, 23, 585– 594. Vallat-Azouvi, C., Pradat-Diehl, P., & Azouvi, P. (2012). The Working Memory Questionnaire: A scale to assess everyday life problems related to deficits of working memory in brain injured patients. Neuropsychological Rehabilitation, 22, 634– 649. Vallat-Azouvi, C., Weber, T., Legrand, L., & Azouvi, P. (2007). Working memory after severe traumatic brain injury. Journal of the International Neuropsychological Society, 13, 770 – 780. Wechsler, D. (1991). WMS-R. Echelle clinique de me´moire de Wechsler-re´vise´e. Paris: Les Editions du Centre de Psychologie Applique´e. Westerberg, H., Jacobaeus, H., Hirvikoski, T., Clevberger, P., Ostensson, M. L., Bartfai, A., & Klingberg, T. (2007). Computerized working memory training after stroke – a pilot study. Brain Injury, 21, 21– 29. Westerberg, H., & Klingberg, T. (2007). Changes in cortical activity after training of working memory – a single-subject analysis. Physiology & Behavior, 92, 186 – 192. Wexler, B. E., Anderson, M., Fulbright, R. K., & Gore, J. C. (2000). Preliminary evidence of improved verbal working memory performance and normalization of task-related frontal lobe activation in schizophrenia following cognitive exercises. American Journal of Psychiatry, 157, 1694 – 1697.
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Downloaded by [University College London] at 11:58 12 November 2014
Wilson, B. A. (1987). Single-case experimental designs in neuropsychological rehabilitation. Journal of Clinical and Experimental Neuropsychology, 9, 527 – 544. Wright, H. H., & Shisler, R. J. (2005). Working memory in aphasia: Theory, measures, and clinical implications. American Journal of Speech-Language Pathology/American Speech-Language-Hearing Association, 14, 107 – 118. Zimmermann, P., & Fimm, B. (2002). A test battery for attentional performance. In M. Leclercq & P. Zimmermann (Eds.), Applied neuropsychology of attention (pp. 110 – 151). London: Psychology Press. Zimmermann, P., & Fimm, B. (2009). TAP: Tests d’e´valuation de l’attention, version 2.2. Adaptation Franc¸aise M. Leclercq. Herzogenrath, Germany: Vera Fimm, Psychologische Testsysteme.
APPENDIX TRAINING TASKS USED FOR REHABILITATION Verbal tasks (Vallat et al., 2005) . .
. . . .
. .
Reconstitution of words from oral spelling: The patient had to reconstruct and pronounce a word that was spelled out by the therapist. Reconstitution of words from oral spelling with a letter omitted: This is the same task as the previous one, but with a letter omitted, replaced by a "bip". Oral spelling. Odd or even number of letters in a word: The task was to find whether the number of letters in a word heard was odd or even. Reconstitution of words from syllables: The therapist presented cluttered syllable words that the subject had to reorder and pronounce. Alphabetic way: The therapist presented a letter and a calculation (addition or subtraction), and the patient had to find the target letter following the increasing or decreasing alphabetical order (for example, B + 6 ¼ H; E – 2 ¼ C). Word sorting in alphabetic order: The patient was required to sort a series of concrete words into alphabetic order. Acronyms: The task was to find out the word made from the initial phonemes of a list of words.
Visuo-spatial tasks (Vallat-Azouvi et al., 2009) . .
2-D mental imagery on a chessboard: The task required patients to move mentally from one position to another on an imagined chessboard. 2-D mental imagery on a calculator keyboard: The task required patients to move mentally from one key to another on an imagined calculator keyboard.
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3-D mental imagery: The task required patients to move mentally from one position to another on an imagined cube. Visual n-back: Three types of stimuli were used: playing cards; figures; geometrical forms. Patients were asked to say whether or not an item matched the item presented 1-, 2- or 3-back in the sequence.
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More demanding executive tasks .
.
.
N-back task-words: This was based on a word semantic categorisation task: series of 20 words were spoken out successively by the therapist, and the patient was asked to respond “yes” when a word was in the same semantic category as the target. Twelve difficulty levels were used, by varying working memory load (1- vs. 2-back), presentation rate (every 1 or 3 seconds), and word length (1, 2 or 3 syllables). N-back task-questions: A series of simple questions was presented verbally by the therapist (such as: “What is the name of the main river in Paris?”). The patient had to give the answer to the question presented one, two or three back in the series depending on the difficulty level. Task difficulty level was also manipulated by varying the presentation rate (every 10 or 5 seconds). If the patient did not know the answer, he was asked to repeat the question. Five series of questions were given per training session. Reading span task: This task was based on Daneman and Carpenter’s (1980) procedure: the patient was asked to read aloud series of sentences and to repeat afterwards the last word of each sentence, in the correct order. Eighteen difficulty levels were used, depending on the number of sentences, but also on sentence length, sentence syntactic complexity, last word length, and word concreteness and imageability.
