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Short-term and working memory impairments in aphasia
Neuropsychologia 49 (2011) 2874–2878
Contents lists available at ScienceDirect
Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia
Short-term and working memory impairments in aphasia Constantin Potagas a , Dimitrios Kasselimis a,b,∗ , Ioannis Evdokimidis a a b
Department of Neurology, National and Kapodistrian University of Athens, Eginition Hospital, Athens, Greece Department of Psychology, University of Crete, Rethymno, Greece
a r t i c l e
i n f o
Article history: Received 10 November 2010 Received in revised form 30 April 2011 Accepted 10 June 2011 Available online 17 June 2011 Keywords: Language disorders Acquired aphasia Digit span Spatial span Short-term memory Working memory
a b s t r a c t The aim of the present study is to investigate short-term memory and working memory deficits in aphasics in relation to the severity of their language impairment. Fifty-eight aphasic patients participated in this study. Based on language assessment, an aphasia score was calculated for each patient. Memory was assessed in two modalities, verbal and spatial. Mean scores for all memory tasks were lower than normal. Aphasia score was significantly correlated with performance on all memory tasks. Correlation coefficients for short-term memory and working memory were approximately of the same magnitude. According to our findings, severity of aphasia is related with both verbal and spatial memory deficits. Moreover, while aphasia score correlated with lower scores in both short-term memory and working memory tasks, the lack of substantial difference between corresponding correlation coefficients suggests a possible primary deficit in information retention rather than impairment in working memory. © 2011 Elsevier Ltd. All rights reserved.
1. Introduction The relationship between language and memory processing has been discussed in several studies (e.g. Howard & Nickels, 2005; Jacquemot & Scott, 2006; Nickels, Howard, & Best, 1997). Moreover, a wide variety of memory deficits has been reported in the aphasia literature. These deficits often implicate short-term memory (STM) (Beeson, Bayles, Rubens, & Kaszniak, 1993; Caramazza, Basili, Koller, & Berndt, 1981; Francis, Clark, & Humphreys, 2003; Friedrich, Martin, & Kemper, 1985; Heilman, Scholes, & Watson, 1978; Koenig-Bruhin & Studer-Eichenberger, 2007; Laures-Gore, Marshall, & Verner, 2011; Martin & Ayala, 2004; Ostergaard & Meudell, 1984) and working memory (WM) (Francis et al., 2003; Kolk & van Grunsven, 1985; Laures-Gore et al., 2011; Miyake, Carpenter, & Just, 1994). STM refers to one’s ability to retain information in consciousness for a short period of time (usually a few seconds) and is a prerequisite for WM, which refers to one’s ability to manipulate the transiently available information. Deficits in both are found in Broca’s as well as in Wernicke’s aphasia (De Renzi & Nichelli, 1975; Ostergaard & Meudell, 1984), transcortical sensory aphasia (Jefferies, Hoffman, Jones, & Lambon Ralph, 2008), and conduction aphasia (Baldo, Klostermann, & Dronkers, 2008; Heilman et al., 1978; Sakurai et al., 1998). Regarding conduction aphasia
∗ Corresponding author at: National and Kapodistrian University of Athens, Eginition Hospital, 74 Vas. Sofias Av., 11528 Athens, Greece. Tel.: +30 2107289307; fax: +30 2107216474. E-mail address: [email protected] (D. Kasselimis). 0028-3932/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2011.06.013
in particular, some authors stress the idea that it is partly a STM disorder (Shallice & Warrington, 1977). Interestingly, such memory deficits in aphasia do not seem to be limited to verbal memory, but they also implicate visuospatial memory. Aphasic patients are found to have an impairment of spatial memory when tested with the Corsi block-tapping task (De Renzi & Nichelli, 1975; Martin & Ayala, 2004). A reduced spatial span has also been reported in individuals suffering from various aphasic syndromes (Albert, 1976). Given that spatial memory is thought to be mainly mediated by right hemisphere structures, such findings seem paradoxical (Burgio & Basso, 1997), but not if one adopts the notion that verbal strategies are necessary to respond in spatial memory tasks (Baldo & Dronkers, 2006). Moreover, memory impairments are associated with left perisylvian lesions involving the inferior parietal lobule, the posterior aspect of the superior temporal gyrus (Wernicke’s area), the middle temporal gyrus, and anterior perisylvian structures including Broca’s area (see Gordon, 1983) that are also implicated in language. However, Burgio and Basso (1997) claim that these memory impairments are independent from the presence of aphasia and are due to lesions of the left cerebral hemisphere in general. In the present study we investigated whether aphasic patients demonstrate STM and WM deficits or not, and if so, in which modality: verbal, spatial, or both. Specifically we addressed three questions: (1) Are aphasic and memory deficits due to a compromized common mechanism? If this were the case, the degree of severity of aphasia would covary with the severity of memory deficits. (2) Does this hypothesized common mechanism specifically concerns the verbal
C. Potagas et al. / Neuropsychologia 49 (2011) 2874–2878
or the spatial material as well? If the memory deficit were specific to language, severity of aphasia would covary only with verbal memory performance; otherwise, it would covary with both verbal and spatial memory performance. (3) Is the common mechanism part of STM or WM? If it were part of STM, severity of aphasia would covary with both STM and WM. If it were part of WM, a stronger correlation would be expected between WM and severity of aphasia. 2. Methods and participants 58 right-handed aphasic patients (15 women), 24–84 years old (mean: 61.33; SD: 13.30), participated in this study. Time post onset (TPO) ranged from 4 to 240 weeks (mean TPO: 58.74 weeks). CT and/or MRI scans were obtained and lesion sites were identified by two independent neuroradiologists. All patients underwent neurological examination. No visual deficit was reported by the neurologist. Each patient was assessed separately by a clinical neuropsychologist. The Boston Diagnostic Aphasia Examination – Short Form (BDAE-SF) adapted in Greek (Tsapkini, Vlahou, & Potagas, 2009) was used for assessing language deficits. Four additional memory tests were administered: WAIS-III digits forward for assessing verbal STM, WAIS-III digits backward for assessing verbal WM, and the Corsi block-tapping task for assessing spatial memory. Memory tests were administered according to standard administration procedures. Any human data included in this manuscript was obtained in compliance with regulations of the Eginition Hospital ethics committee. In the present study, specific BDAE-SF subtests were used: the auditory sentence comprehension subtest, and the oral expression subtest. In the auditory sentence comprehension subtest, the patient is asked to execute a command spoken by the examiner. The stimuli range from simple (e.g. a two-item command, such as “show me the ceiling, and then the floor”, where the patient receives a maximum of a twopoint score) to more complex commands (e.g. a five-item command, such as “tap each shoulder twice with two fingers, while keeping your eyes closed”, where the patient receives a maximum of a five-point score). In the oral expression subtest, the patient is asked to describe what happened to him/her (stroke story). In the present study, the stroke story was recorded and then speech rate (words/minute) was calculated for each patient, by two independent judges (inter-rater consistency: r = 0.98, p < 0.001).
2.1. Calculation of the aphasia score BDAE-SF already includes an aphasia severity scale. However, it is a qualitative six-point scale, thus offering little information. That is why we decided to create a simple aphasia score, based on the auditory sentence comprehension subtest, and the oral expression subtest, since comprehension and fluency are the most efficient indices of aphasia severity (Goodglass & Kaplan, 1972). Since it is methodologically incorrect to add scores that are not related with each other in any way, we explored the possibility of a relationship between the two scores. Analyses using Pearson r revealed a statistically significant correlation between scores in the two language subtests (r = 0.48, p < 0.001). This allowed the calculation of a total aphasia score (AS). The scores of the two BDAE-SF subtests were adjusted, so as to range between 0 and 10. We defined AS as the total (adjusted score for fluency plus adjusted score for comprehension).
3. Results and discussion Every patient’s span length, span score (number of correctly remembered trials), and product score (the product of the span length and the number of correctly remembered trials) were calculated for each test, according to Kessels, van den Berg, Ruis, and Brands (2008). Individual patients’ span product scores and AS are shown in Table 1. It could be speculated that a severe fluency deficit would result in an extremely low verbal span score, even in the absence of any memory disorder (Burgio & Basso, 1997). If a patient with no memory deficit cannot produce speech, then he/she will be unable to repeat even one or two digits, thus scoring extremely low in the digit span test. Therefore, he/she will be wrongly classified as a patient with a verbal memory deficit, while his/her low span should not be attributed to memory impairment. Moreover, severely impaired comprehension can result in misleading scores regarding almost any test of cognitive ability. If a patient cannot understand what he/she is asked to do, then his/her performance will be diminished, but this reduced score should be attributed to a comprehension, rather than a memory deficit.
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In order to avoid such a confounding due to aphasic deficits regarding comprehension and speech output, patients with severe language deficits were excluded, before conducting the statistical analyses. For digit span forward and backward, patients who could not repeat at least one 2-syllable word (of the BDAE-SF word repetition subtest) or lacked the ability to execute a simple, one-item command (from the BDAE-SF sentence comprehension subtest) were excluded (patients 7, 15, 19, 24, 28, 32, 33, 34, 42, 45, 46, 49, 51, 52). Thus, 44 patients (11 women), 24–84 years old (mean: 59.77; SD: 14.42) were finally included in the analyses regarding digit span forward and backward (mean TPO: 60.04 weeks). For the Corsi block-tapping task, since a verbal response is not required, only patients who could not execute a simple, one-item command (from the BDAE-SF sentence comprehension subtest) were excluded (patients 15, 24, 45, 49). In this case, 54 patients (14 women), 24–84 years old (mean: 61.15; SD: 13.66) were finally included in the analyses regarding Corsi block-tapping task (mean TPO: 60.60 weeks). One-sample t-tests revealed lower than expected product scores for all memory tasks [critical value for forward digit span: 50 (t = −18.054, p < 0.001), critical value for backward digit span: 26 (t = −17.272, p < 0.001), critical value for spatial forward span: 38 (t = −3.832, p < 0.001), critical value for backward spatial span: 38 (t = −9.626, p < 0.001)]. Critical values were decided on the basis of normative data by Kessels et al. (2008), where mean performances for 246 healthy older adults were presented. Means and standard deviations for patients’ scores are shown in Table 2. Given that the age range in our sample is quite large and that memory declines with age in the normal population, it could be proposed that separate norms should be used for different age groups. However, such norms were not used for each individual aphasic in our sample for several reasons. First of all, Kessels et al. (2008) found that age and education related effects were below 0.30 which is rather small (Cohen, 1992). Secondly, they did not find a gender effect. Moreover, the main aim of this study is not to demonstrate memory deficits in aphasic patients, but to investigate the possible relations between performance in memory tasks and severity of aphasia. For the aforementioned reasons we concluded that there was no need for using separate norms and therefore we did set a critical value for each t-test based on the normative data provided in Kessels et al. (2008). However, correlation analyses in our study were performed with age and education as control variables (see below). The deficits found in our aphasic sample are not specific to verbal modality, because our patients showed impaired performance in the verbal and the spatial memory tests. Deficits in overall visual memory have also been found in other studies (Locke & Deck, 1978; Ostergaard & Meudell, 1984). Moreover, low performances are reported regarding Corsi block tapping task in particular (De Renzi & Nichelli, 1975; Martin & Ayala, 2004). One should keep in mind, though, that a group of 58 aphasic patients cannot be considered as a homogenous group and the interpretation of group data needs some caution. In order to avoid bias, we did not select specific patients, but only excluded the ones that could not perform the task due to language problems. As can be seen in Table 1, some patients suffer from verbal memory deficits, others from spatial memory deficits, others from both, and others do not. The main aim of this study was to explore possible relationships between linguistic and memory deficits in aphasic patients. Partial correlations were calculated between AS and product scores in the four memory tasks controlling for age and years of formal schooling. AS was significantly correlated with patients’ performances in WM and STM tasks, and in both modalities, verbal and spatial (Table 3). The correlation was stronger for verbal memory than for spatial memory tasks. However, correlation coefficients between WM
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Table 1 Span product scores and AS for each patient. Patients
Age
TPO (weeks)
WAIS-III digits forward (product score) Maximum score: 144
WAIS-III digits backward (product score) Maximum score: 112
Corsi forward (product score) Maximum score: 144
Corsi backward (product score) Maximum score: 112
AS max: 20
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58
64 45 38 56 50 55 52 50 52 73 54 61 74 57 60 71 76 59 66 59 79 84 76 57 60 78 67 62 54 56 59 72 63 73 49 78 61 74 63 79 35 79 74 55 64 67 51 58 74 72 72 66 75 31 24 45 32 67
44 221 37 12 87 27 24 29 9 43 84 21 18 109 12 73 80 11 33 45 11 4 36 11 11 176 240 76 35 145 71 111 145 56 99 15 8 52 34 33 25 30 4 6 52 18 39 98 80 195 107 27 133 9 21 82 73 20
12 0 6 20 24 24 0 2 35 12 12 48 20 0 0 4 12 16 0 0 4 20 0 4 24 24 2 0 0 2 24 0 0 40 12 24 9 4 6 4 20 0 24 9 0 0 24 9 0 4 0 12 16 63 20 12 2 24
16 0 0 12 2 9 0 0 12 9 9 20 6 0 0 0 0 2 0 0 9 2 0 2 0 20 0 0 0 0 9 0 0 6 9 9 4 2 0 0 16 0 9 4 0 0 2 6 0 4 0 2 9 20 9 9 0 35
35 20 24 35 24 77 30 20 40 35 60 48 30 0 16 35 6 30 16 24 20 60 0 9 20 24 35 20 24 35 20 4 24 30 54 16 35 16 24 54 20 9 35 48 9 20 48 42 0 48 2 20 20 48 63 20 4 24
24 35 20 63 16 25 24 12 24 16 20 24 16 0 0 4 0 16 20 20 4 20 0 16 9 20 16 12 12 16 24 4 2 4 16 4 20 4 4 24 30 0 24 24 0 16 35 48 0 25 2 16 16 60 54 24 40 24
18 11 7 14 11 14 7 5 18 17 16 16 18 6 1 19 12 10 4 11 11 17 10 4 9 17 10 3 9 5 20 12 4 11 15 18 20 14 12 10 20 9 16 6 0 1 12 17 0 15 2 17 18 20 18 10 5 19
Table 2 One sample t-test for the four memory subtests. Critical value
Mean
SD
WAIS-III digits forward (product score)
50
13.09
WAIS-III digits backward (product score)
26
Corsi forward (product score)
38
Corsi backward (product score)
38
14.39*** (N = 44) 6.45*** (N = 44) 29.17*** (N = 54) 19.11*** (N = 54)
***
p < 0.001.
7.51 16.94 14.42
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Table 3 Partial correlations between AS and product scores in the four memory tasks controlling for age and years of formal schooling. Aphasia score Aphasia score WAIS-III digits forward WAIS-III digits backward Corsi forward Corsi backward * ** ***
1.00 0.514** (N = 44) 0.59*** (N = 44) 0.36* (N = 54) 0.33* (N = 54)
WAIS-III digits forward
WAIS-III digits backward
Corsi forward
Corsi backward
1.00 0.59*** (N = 44) 0.24 (N = 44) 0.21 (N = 44)
1.00 0.11 (N = 44) 0.27 (N = 44)
1.00 0.43** (N = 54)
1.00
p < 0.05. p < 0.01. p < 0.001.
and STM measures are approximately of the same magnitude. Our results are in accordance with Laures-Gore et al. (2011), who found that forward and backward digit span scores were strongly correlated with severity of aphasia. Our first hypothesis was that if aphasic and memory deficits are due to a compromized common mechanism, severity of language deficits would covary with the degree of memory impairments. Our results show that this is actually the case, since AS is significantly correlated with patients’ performance in all four memory tasks. AS is calculated in such a way, that greater scores mean better performance in the language tasks. Thus, given that there is a positive correlation between AS and scores in the four memory tasks, our findings support the validity of our first hypothesis, indicating a covariance between memory and language deficits. Our second question relates to the possible involvement of several memory modalities affected in aphasia. Our data show significant correlations of AS with both verbal and spatial memory scores. This finding is rather interesting, considering that our patients’ lesions are located in the left hemisphere and spatial memory is thought to be more sensitive to right hemisphere lesions (De Renzi & Nichelli, 1975). According to Burgio and Basso (1997) “the effect of the left-hemisphere lesion on the vast majority of memory tests and particularly on the spatial memory tests remains, however, unexplained” (p. 765). On the other hand, it has been argued that the left hemisphere is dominant for processing or storing of successive stimuli, independently of modality (Baldo & Dronkers, 2006; Chein, Ravizza, & Fiez, 2003). Another explanation would be the engagement of masked verbal strategies for recall of spatial stimuli. However, deficits in visual memory have been found in studies, where stimuli were difficult to translate into words (Ostergaard & Meudell, 1984). In our sample 15 patients demonstrate both verbal and spatial memory deficits, indicating a modality-independent memory deficit proportional in severity with the language deficit (see Table 1: patients 5, 8, 14, 16, 17, 18, 21, 25, 27, 29, 30, 35, 38, 39, 53). It should be noted, however, that spatial and verbal memory scores do not correlate significantly with each other. This finding may pose limitations to our hypothesis on the underlying common mechanism affecting language and memory. But the patients reported having both verbal and spatial memory deficits were very few (15 out of 58) to establish a robust relationship between language and memory, independently of modality. Further research with greater aphasic samples could elucidate this issue. The third question we examined in this study was whether the putative common mechanism which is found to be compromised, is part of STM or of WM. Kessels et al. (2008) argue that since the Corsi backward is characterized by the same degree of difficulty as the Corsi forward (a phenomenon not occurring when individuals are tested with digit recall, backward and for-
ward), it is unclear whether this visuospatial Corsi subtest actually corresponds to WM functions. The authors corroborate the idea that the Corsi Block-Tapping Task backward task may rely on processing within working-memory’s slave systems, rather than the central executive. In contrast, the difference concerning difficulty between digit span forward and backward (with the latter being more difficult), somewhat proves that digit span backward relies on the central executive component of working memory, while digit span forward possibly involves WM slave systems. However, it should be noted that the pattern found by Kessels et al. (2008) in healthy participants was not replicated in our aphasic population. Our patients performed significantly worse in the Corsi backward in comparison with the Corsi forward. Paired sample t-test between product scores for the Corsi backward and the Corsi forward revealed a statistical significant difference (t = 4.744, p < 0.001). Nevertheless, in the present study, the answer to the third question relies on the data from the verbal span. Our results show that AS is significantly correlated with both STM and WM, while correlation coefficients are approximately the same within the verbal modality. This implies that the primary deficit concerns simply maintenance of information, rather than ability to manipulate it (i.e. working memory). Impaired processing could of course occur secondarily, due to the presumed STM disorder. Our data are at variance with the position of Dick et al. (2001), who argued that the impairment in aphasia is mainly associated with incoming information load. In this context, an aphasic’s ability to process information is not totally abolished, but reduced in such manner that when stimuli are presented rapidly in the presence of interference, performance declines. However, this does not seem to be the case with our patients, since our data indicate that the primary deficit concerns STM, rather than WM. 4. Conclusion In the present study, we tested three related hypotheses. 1st: That aphasic and memory deficits are due to a compromized common mechanism. 2nd: That this common mechanism concerns memory for verbal and spatial stimuli. 3rd: That this common mechanism is part of STM. We found that memory scores correlated with AS in both stimulus modalities, spatial and verbal. However, the correlation coefficients for STM and WM did not differ. Therefore, these data support the hypothesis of a common mechanism underlying aphasia and memory deficits (and not linguistic deficits only). Moreover, and with regard to our second hypothesis, the statistically significant correlations found for both verbal and spatial tasks, indicate that this mechanism should be stimulus modality-independent. Finally, regarding our third hypothesis, this
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hypothesized mechanism seems to rely on STM, given that correlation coefficients for STM and WM are approximately the same. Funding This research received no specific grant from any funding agency, commercial or not-for-profit sectors. References Albert, M. L. (1976). Short-term memory and aphasia. Brain and Language, 3, 28–33. Baldo, J. V., & Dronkers, N. F. (2006). The role of inferior parietal and inferior frontal cortex in working memory. Neuropsychology, 20, 529–538. Baldo, J. V., Klostermann, E. C., & Dronkers, N. F. (2008). It’s either a cook or a baker: Patients with conduction aphasia get the gist but lose the trace. Brain and Language, 105(2), 134–140. Beeson, P. M., Bayles, K. A., Rubens, A. W., & Kaszniak, A. W. (1993). Memory impairment and executive control in individuals with stroke-induced aphasia. Brain and Language, 45, 253–275. Burgio, F., & Basso, A. (1997). Memory and aphasia. Neuropsychologia, 35, 759–766. Caramazza, A., Basili, A. G., Koller, J. J., & Berndt, R. S. (1981). An investigation of repetition and language processing in a case of conduction aphasia. Brain and Language, 14, 235–271. Chein, J. M., Ravizza, S. M., & Fiez, J. A. (2003). Using neuroimaging to evaluate models of working memory and their implications for language processing. Journal of Neurolinguistics, 16, 315–339. Cohen, J. (1992). A power primer. Psychological Bulletin, 112, 155–159. De Renzi, E., & Nichelli, P. (1975). Verbal and non!verbal term memory impairment following hemispheric damage. Cortex, 11, 341–354. Dick, F., Bates, E., Wulfeck, B., Utman, J. A., Dronkers, N., & Gernsbacher, M. A. (2001). Language deficits, localization, and grammar: Evidence for a distributive model of language breakdown in aphasic patients and neurologically intact individuals. Psychological Review, 108, 759–788. Francis, D. R., Clark, N., & Humphreys, G. W. (2003). The treatment of an auditory working memory deficit and the implications for sentence comprehension abilities in mild “receptive” aphasia. Aphasiology, 17(8), 723–750. Friedrich, F. J., Martin, R., & Kemper, S. J. (1985). Consequences of a phonological decoding deficit on sentence processing. Cognitive Neuropsychology, 2, 385– 412. Goodglass, H., & Kaplan, E. (1972). The assessment of aphasia and related disorders. Philadelphia, PA: Lea & Febiger. Gordon, W. P. (1983). Memory disorders in aphasia. I. Auditory immediate recall. Neuropsychologia, 21, 325–339.
Heilman, K. A., Scholes, R., & Watson, R. T. (1978). Defects of immediate memory in Broca’s and conduction aphasia. Brain and Language, 3, 201–209. Howard, D., & Nickels, L. (2005). Separating input and output phonology: Semantic, phonological, and orthographic effects in short-term memory impairment. Cognitive Neuropsychology, 22(1), 42–77. Jacquemot, C., & Scott, S. K. (2006). What is the relationship between phonological short-term memory and speech processing? Trends in Cognitive Science, 10(11), 480–486. Jefferies, E., Hoffman, P., Jones, R., & Lambon Ralph, M. A. (2008). The impact of semantic impairment on verbal short-term memory in stroke aphasia and semantic dementia: A comparative study. Journal of Memory and Language, 58, 66–87. Kessels, R. P. C., van den Berg, E., Ruis, C., & Brands, A. M. A. (2008). The backward span of the Corsi Block-Tapping Task and its association with the WAIS-III digit span. Assessment, 15, 426–434. Koenig-Bruhin, M., & Studer-Eichenberger, F. (2007). Therapy of short-term memory disorders in fluent aphasia: A single case study. Aphasiology, 21(5), 448–458. Kolk, H. H. J., & van Grunsven, M. M. F. (1985). Agrammatism as a variable phenomenon. Cognitive Neuropsychology, 2, 347–384. Laures-Gore, J. S., Marshall, R. S., & Verner, E. (2011). Performance of individuals with left hemisphere stroke and aphasia and individuals with right brain damage on forward and backward digit span tasks. Aphasiology, 25(1), 43–56. Locke, J. L., & Deck, J. W. (1978). Retrieval failure, rehearsal deficiency, and short-term memory loss in the aphasic adult. Brain and Language, 5, 227–235. Martin, N., & Ayala, J. (2004). Measurements of auditory-verbal STM span in aphasia: Effects of item, task, and lexical impairment. Brain and Language, 89(3), 464–483. Miyake, A., Carpenter, P. A., & Just, M. A. (1994). A capacity approach to syntactic comprehension disorders: Making normal adults perform like aphasics. Cognitive Neuropsychology, 11, 671–717. Nickels, L., Howard, D., & Best, W. (1997). Fractionating the articulatory loop: Dissociations and associations in phonological recoding in aphasia. Brain and Language, 56(2), 161–182. Ostergaard, A. L., & Meudell, P. R. (1984). Immediate memory span, recognition memory for subspan series of words, and serial position effects in recognition memory for supraspan series of verbal and nonverbal items in Broca’s and Wernicke’s aphasia. Brain and Language, 22, 1–13. Sakurai, Y., Takeuchi, S., Kojima, E., Yazawa, I., Murayama, S., Kaga, K., et al. (1998). Mechanism of short-term memory and repetition in conduction aphasia and related cognitive disorders: A neuropsychological, audiological and neuroimaging study. Journal of the Neurological Sciences, 154(2), 182–193. Shallice, T., & Warrington, E. K. (1977). Auditory-verbal short-term memory impairment and conduction aphasia. Brain and Language, 4, 479–491. Tsapkini, K., Vlahou, C. H., & Potagas, C. (2009). Adaptation and validation of standardized aphasia tests in different languages: Lessons from the Boston Diagnostic Aphasia Examination – Short Form in Greek. Behavioural Neurology, 22, 111–119.
Contents lists available at ScienceDirect
Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia
Short-term and working memory impairments in aphasia Constantin Potagas a , Dimitrios Kasselimis a,b,∗ , Ioannis Evdokimidis a a b
Department of Neurology, National and Kapodistrian University of Athens, Eginition Hospital, Athens, Greece Department of Psychology, University of Crete, Rethymno, Greece
a r t i c l e
i n f o
Article history: Received 10 November 2010 Received in revised form 30 April 2011 Accepted 10 June 2011 Available online 17 June 2011 Keywords: Language disorders Acquired aphasia Digit span Spatial span Short-term memory Working memory
a b s t r a c t The aim of the present study is to investigate short-term memory and working memory deficits in aphasics in relation to the severity of their language impairment. Fifty-eight aphasic patients participated in this study. Based on language assessment, an aphasia score was calculated for each patient. Memory was assessed in two modalities, verbal and spatial. Mean scores for all memory tasks were lower than normal. Aphasia score was significantly correlated with performance on all memory tasks. Correlation coefficients for short-term memory and working memory were approximately of the same magnitude. According to our findings, severity of aphasia is related with both verbal and spatial memory deficits. Moreover, while aphasia score correlated with lower scores in both short-term memory and working memory tasks, the lack of substantial difference between corresponding correlation coefficients suggests a possible primary deficit in information retention rather than impairment in working memory. © 2011 Elsevier Ltd. All rights reserved.
1. Introduction The relationship between language and memory processing has been discussed in several studies (e.g. Howard & Nickels, 2005; Jacquemot & Scott, 2006; Nickels, Howard, & Best, 1997). Moreover, a wide variety of memory deficits has been reported in the aphasia literature. These deficits often implicate short-term memory (STM) (Beeson, Bayles, Rubens, & Kaszniak, 1993; Caramazza, Basili, Koller, & Berndt, 1981; Francis, Clark, & Humphreys, 2003; Friedrich, Martin, & Kemper, 1985; Heilman, Scholes, & Watson, 1978; Koenig-Bruhin & Studer-Eichenberger, 2007; Laures-Gore, Marshall, & Verner, 2011; Martin & Ayala, 2004; Ostergaard & Meudell, 1984) and working memory (WM) (Francis et al., 2003; Kolk & van Grunsven, 1985; Laures-Gore et al., 2011; Miyake, Carpenter, & Just, 1994). STM refers to one’s ability to retain information in consciousness for a short period of time (usually a few seconds) and is a prerequisite for WM, which refers to one’s ability to manipulate the transiently available information. Deficits in both are found in Broca’s as well as in Wernicke’s aphasia (De Renzi & Nichelli, 1975; Ostergaard & Meudell, 1984), transcortical sensory aphasia (Jefferies, Hoffman, Jones, & Lambon Ralph, 2008), and conduction aphasia (Baldo, Klostermann, & Dronkers, 2008; Heilman et al., 1978; Sakurai et al., 1998). Regarding conduction aphasia
∗ Corresponding author at: National and Kapodistrian University of Athens, Eginition Hospital, 74 Vas. Sofias Av., 11528 Athens, Greece. Tel.: +30 2107289307; fax: +30 2107216474. E-mail address: [email protected] (D. Kasselimis). 0028-3932/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2011.06.013
in particular, some authors stress the idea that it is partly a STM disorder (Shallice & Warrington, 1977). Interestingly, such memory deficits in aphasia do not seem to be limited to verbal memory, but they also implicate visuospatial memory. Aphasic patients are found to have an impairment of spatial memory when tested with the Corsi block-tapping task (De Renzi & Nichelli, 1975; Martin & Ayala, 2004). A reduced spatial span has also been reported in individuals suffering from various aphasic syndromes (Albert, 1976). Given that spatial memory is thought to be mainly mediated by right hemisphere structures, such findings seem paradoxical (Burgio & Basso, 1997), but not if one adopts the notion that verbal strategies are necessary to respond in spatial memory tasks (Baldo & Dronkers, 2006). Moreover, memory impairments are associated with left perisylvian lesions involving the inferior parietal lobule, the posterior aspect of the superior temporal gyrus (Wernicke’s area), the middle temporal gyrus, and anterior perisylvian structures including Broca’s area (see Gordon, 1983) that are also implicated in language. However, Burgio and Basso (1997) claim that these memory impairments are independent from the presence of aphasia and are due to lesions of the left cerebral hemisphere in general. In the present study we investigated whether aphasic patients demonstrate STM and WM deficits or not, and if so, in which modality: verbal, spatial, or both. Specifically we addressed three questions: (1) Are aphasic and memory deficits due to a compromized common mechanism? If this were the case, the degree of severity of aphasia would covary with the severity of memory deficits. (2) Does this hypothesized common mechanism specifically concerns the verbal
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or the spatial material as well? If the memory deficit were specific to language, severity of aphasia would covary only with verbal memory performance; otherwise, it would covary with both verbal and spatial memory performance. (3) Is the common mechanism part of STM or WM? If it were part of STM, severity of aphasia would covary with both STM and WM. If it were part of WM, a stronger correlation would be expected between WM and severity of aphasia. 2. Methods and participants 58 right-handed aphasic patients (15 women), 24–84 years old (mean: 61.33; SD: 13.30), participated in this study. Time post onset (TPO) ranged from 4 to 240 weeks (mean TPO: 58.74 weeks). CT and/or MRI scans were obtained and lesion sites were identified by two independent neuroradiologists. All patients underwent neurological examination. No visual deficit was reported by the neurologist. Each patient was assessed separately by a clinical neuropsychologist. The Boston Diagnostic Aphasia Examination – Short Form (BDAE-SF) adapted in Greek (Tsapkini, Vlahou, & Potagas, 2009) was used for assessing language deficits. Four additional memory tests were administered: WAIS-III digits forward for assessing verbal STM, WAIS-III digits backward for assessing verbal WM, and the Corsi block-tapping task for assessing spatial memory. Memory tests were administered according to standard administration procedures. Any human data included in this manuscript was obtained in compliance with regulations of the Eginition Hospital ethics committee. In the present study, specific BDAE-SF subtests were used: the auditory sentence comprehension subtest, and the oral expression subtest. In the auditory sentence comprehension subtest, the patient is asked to execute a command spoken by the examiner. The stimuli range from simple (e.g. a two-item command, such as “show me the ceiling, and then the floor”, where the patient receives a maximum of a twopoint score) to more complex commands (e.g. a five-item command, such as “tap each shoulder twice with two fingers, while keeping your eyes closed”, where the patient receives a maximum of a five-point score). In the oral expression subtest, the patient is asked to describe what happened to him/her (stroke story). In the present study, the stroke story was recorded and then speech rate (words/minute) was calculated for each patient, by two independent judges (inter-rater consistency: r = 0.98, p < 0.001).
2.1. Calculation of the aphasia score BDAE-SF already includes an aphasia severity scale. However, it is a qualitative six-point scale, thus offering little information. That is why we decided to create a simple aphasia score, based on the auditory sentence comprehension subtest, and the oral expression subtest, since comprehension and fluency are the most efficient indices of aphasia severity (Goodglass & Kaplan, 1972). Since it is methodologically incorrect to add scores that are not related with each other in any way, we explored the possibility of a relationship between the two scores. Analyses using Pearson r revealed a statistically significant correlation between scores in the two language subtests (r = 0.48, p < 0.001). This allowed the calculation of a total aphasia score (AS). The scores of the two BDAE-SF subtests were adjusted, so as to range between 0 and 10. We defined AS as the total (adjusted score for fluency plus adjusted score for comprehension).
3. Results and discussion Every patient’s span length, span score (number of correctly remembered trials), and product score (the product of the span length and the number of correctly remembered trials) were calculated for each test, according to Kessels, van den Berg, Ruis, and Brands (2008). Individual patients’ span product scores and AS are shown in Table 1. It could be speculated that a severe fluency deficit would result in an extremely low verbal span score, even in the absence of any memory disorder (Burgio & Basso, 1997). If a patient with no memory deficit cannot produce speech, then he/she will be unable to repeat even one or two digits, thus scoring extremely low in the digit span test. Therefore, he/she will be wrongly classified as a patient with a verbal memory deficit, while his/her low span should not be attributed to memory impairment. Moreover, severely impaired comprehension can result in misleading scores regarding almost any test of cognitive ability. If a patient cannot understand what he/she is asked to do, then his/her performance will be diminished, but this reduced score should be attributed to a comprehension, rather than a memory deficit.
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In order to avoid such a confounding due to aphasic deficits regarding comprehension and speech output, patients with severe language deficits were excluded, before conducting the statistical analyses. For digit span forward and backward, patients who could not repeat at least one 2-syllable word (of the BDAE-SF word repetition subtest) or lacked the ability to execute a simple, one-item command (from the BDAE-SF sentence comprehension subtest) were excluded (patients 7, 15, 19, 24, 28, 32, 33, 34, 42, 45, 46, 49, 51, 52). Thus, 44 patients (11 women), 24–84 years old (mean: 59.77; SD: 14.42) were finally included in the analyses regarding digit span forward and backward (mean TPO: 60.04 weeks). For the Corsi block-tapping task, since a verbal response is not required, only patients who could not execute a simple, one-item command (from the BDAE-SF sentence comprehension subtest) were excluded (patients 15, 24, 45, 49). In this case, 54 patients (14 women), 24–84 years old (mean: 61.15; SD: 13.66) were finally included in the analyses regarding Corsi block-tapping task (mean TPO: 60.60 weeks). One-sample t-tests revealed lower than expected product scores for all memory tasks [critical value for forward digit span: 50 (t = −18.054, p < 0.001), critical value for backward digit span: 26 (t = −17.272, p < 0.001), critical value for spatial forward span: 38 (t = −3.832, p < 0.001), critical value for backward spatial span: 38 (t = −9.626, p < 0.001)]. Critical values were decided on the basis of normative data by Kessels et al. (2008), where mean performances for 246 healthy older adults were presented. Means and standard deviations for patients’ scores are shown in Table 2. Given that the age range in our sample is quite large and that memory declines with age in the normal population, it could be proposed that separate norms should be used for different age groups. However, such norms were not used for each individual aphasic in our sample for several reasons. First of all, Kessels et al. (2008) found that age and education related effects were below 0.30 which is rather small (Cohen, 1992). Secondly, they did not find a gender effect. Moreover, the main aim of this study is not to demonstrate memory deficits in aphasic patients, but to investigate the possible relations between performance in memory tasks and severity of aphasia. For the aforementioned reasons we concluded that there was no need for using separate norms and therefore we did set a critical value for each t-test based on the normative data provided in Kessels et al. (2008). However, correlation analyses in our study were performed with age and education as control variables (see below). The deficits found in our aphasic sample are not specific to verbal modality, because our patients showed impaired performance in the verbal and the spatial memory tests. Deficits in overall visual memory have also been found in other studies (Locke & Deck, 1978; Ostergaard & Meudell, 1984). Moreover, low performances are reported regarding Corsi block tapping task in particular (De Renzi & Nichelli, 1975; Martin & Ayala, 2004). One should keep in mind, though, that a group of 58 aphasic patients cannot be considered as a homogenous group and the interpretation of group data needs some caution. In order to avoid bias, we did not select specific patients, but only excluded the ones that could not perform the task due to language problems. As can be seen in Table 1, some patients suffer from verbal memory deficits, others from spatial memory deficits, others from both, and others do not. The main aim of this study was to explore possible relationships between linguistic and memory deficits in aphasic patients. Partial correlations were calculated between AS and product scores in the four memory tasks controlling for age and years of formal schooling. AS was significantly correlated with patients’ performances in WM and STM tasks, and in both modalities, verbal and spatial (Table 3). The correlation was stronger for verbal memory than for spatial memory tasks. However, correlation coefficients between WM
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Table 1 Span product scores and AS for each patient. Patients
Age
TPO (weeks)
WAIS-III digits forward (product score) Maximum score: 144
WAIS-III digits backward (product score) Maximum score: 112
Corsi forward (product score) Maximum score: 144
Corsi backward (product score) Maximum score: 112
AS max: 20
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58
64 45 38 56 50 55 52 50 52 73 54 61 74 57 60 71 76 59 66 59 79 84 76 57 60 78 67 62 54 56 59 72 63 73 49 78 61 74 63 79 35 79 74 55 64 67 51 58 74 72 72 66 75 31 24 45 32 67
44 221 37 12 87 27 24 29 9 43 84 21 18 109 12 73 80 11 33 45 11 4 36 11 11 176 240 76 35 145 71 111 145 56 99 15 8 52 34 33 25 30 4 6 52 18 39 98 80 195 107 27 133 9 21 82 73 20
12 0 6 20 24 24 0 2 35 12 12 48 20 0 0 4 12 16 0 0 4 20 0 4 24 24 2 0 0 2 24 0 0 40 12 24 9 4 6 4 20 0 24 9 0 0 24 9 0 4 0 12 16 63 20 12 2 24
16 0 0 12 2 9 0 0 12 9 9 20 6 0 0 0 0 2 0 0 9 2 0 2 0 20 0 0 0 0 9 0 0 6 9 9 4 2 0 0 16 0 9 4 0 0 2 6 0 4 0 2 9 20 9 9 0 35
35 20 24 35 24 77 30 20 40 35 60 48 30 0 16 35 6 30 16 24 20 60 0 9 20 24 35 20 24 35 20 4 24 30 54 16 35 16 24 54 20 9 35 48 9 20 48 42 0 48 2 20 20 48 63 20 4 24
24 35 20 63 16 25 24 12 24 16 20 24 16 0 0 4 0 16 20 20 4 20 0 16 9 20 16 12 12 16 24 4 2 4 16 4 20 4 4 24 30 0 24 24 0 16 35 48 0 25 2 16 16 60 54 24 40 24
18 11 7 14 11 14 7 5 18 17 16 16 18 6 1 19 12 10 4 11 11 17 10 4 9 17 10 3 9 5 20 12 4 11 15 18 20 14 12 10 20 9 16 6 0 1 12 17 0 15 2 17 18 20 18 10 5 19
Table 2 One sample t-test for the four memory subtests. Critical value
Mean
SD
WAIS-III digits forward (product score)
50
13.09
WAIS-III digits backward (product score)
26
Corsi forward (product score)
38
Corsi backward (product score)
38
14.39*** (N = 44) 6.45*** (N = 44) 29.17*** (N = 54) 19.11*** (N = 54)
***
p < 0.001.
7.51 16.94 14.42
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Table 3 Partial correlations between AS and product scores in the four memory tasks controlling for age and years of formal schooling. Aphasia score Aphasia score WAIS-III digits forward WAIS-III digits backward Corsi forward Corsi backward * ** ***
1.00 0.514** (N = 44) 0.59*** (N = 44) 0.36* (N = 54) 0.33* (N = 54)
WAIS-III digits forward
WAIS-III digits backward
Corsi forward
Corsi backward
1.00 0.59*** (N = 44) 0.24 (N = 44) 0.21 (N = 44)
1.00 0.11 (N = 44) 0.27 (N = 44)
1.00 0.43** (N = 54)
1.00
p < 0.05. p < 0.01. p < 0.001.
and STM measures are approximately of the same magnitude. Our results are in accordance with Laures-Gore et al. (2011), who found that forward and backward digit span scores were strongly correlated with severity of aphasia. Our first hypothesis was that if aphasic and memory deficits are due to a compromized common mechanism, severity of language deficits would covary with the degree of memory impairments. Our results show that this is actually the case, since AS is significantly correlated with patients’ performance in all four memory tasks. AS is calculated in such a way, that greater scores mean better performance in the language tasks. Thus, given that there is a positive correlation between AS and scores in the four memory tasks, our findings support the validity of our first hypothesis, indicating a covariance between memory and language deficits. Our second question relates to the possible involvement of several memory modalities affected in aphasia. Our data show significant correlations of AS with both verbal and spatial memory scores. This finding is rather interesting, considering that our patients’ lesions are located in the left hemisphere and spatial memory is thought to be more sensitive to right hemisphere lesions (De Renzi & Nichelli, 1975). According to Burgio and Basso (1997) “the effect of the left-hemisphere lesion on the vast majority of memory tests and particularly on the spatial memory tests remains, however, unexplained” (p. 765). On the other hand, it has been argued that the left hemisphere is dominant for processing or storing of successive stimuli, independently of modality (Baldo & Dronkers, 2006; Chein, Ravizza, & Fiez, 2003). Another explanation would be the engagement of masked verbal strategies for recall of spatial stimuli. However, deficits in visual memory have been found in studies, where stimuli were difficult to translate into words (Ostergaard & Meudell, 1984). In our sample 15 patients demonstrate both verbal and spatial memory deficits, indicating a modality-independent memory deficit proportional in severity with the language deficit (see Table 1: patients 5, 8, 14, 16, 17, 18, 21, 25, 27, 29, 30, 35, 38, 39, 53). It should be noted, however, that spatial and verbal memory scores do not correlate significantly with each other. This finding may pose limitations to our hypothesis on the underlying common mechanism affecting language and memory. But the patients reported having both verbal and spatial memory deficits were very few (15 out of 58) to establish a robust relationship between language and memory, independently of modality. Further research with greater aphasic samples could elucidate this issue. The third question we examined in this study was whether the putative common mechanism which is found to be compromised, is part of STM or of WM. Kessels et al. (2008) argue that since the Corsi backward is characterized by the same degree of difficulty as the Corsi forward (a phenomenon not occurring when individuals are tested with digit recall, backward and for-
ward), it is unclear whether this visuospatial Corsi subtest actually corresponds to WM functions. The authors corroborate the idea that the Corsi Block-Tapping Task backward task may rely on processing within working-memory’s slave systems, rather than the central executive. In contrast, the difference concerning difficulty between digit span forward and backward (with the latter being more difficult), somewhat proves that digit span backward relies on the central executive component of working memory, while digit span forward possibly involves WM slave systems. However, it should be noted that the pattern found by Kessels et al. (2008) in healthy participants was not replicated in our aphasic population. Our patients performed significantly worse in the Corsi backward in comparison with the Corsi forward. Paired sample t-test between product scores for the Corsi backward and the Corsi forward revealed a statistical significant difference (t = 4.744, p < 0.001). Nevertheless, in the present study, the answer to the third question relies on the data from the verbal span. Our results show that AS is significantly correlated with both STM and WM, while correlation coefficients are approximately the same within the verbal modality. This implies that the primary deficit concerns simply maintenance of information, rather than ability to manipulate it (i.e. working memory). Impaired processing could of course occur secondarily, due to the presumed STM disorder. Our data are at variance with the position of Dick et al. (2001), who argued that the impairment in aphasia is mainly associated with incoming information load. In this context, an aphasic’s ability to process information is not totally abolished, but reduced in such manner that when stimuli are presented rapidly in the presence of interference, performance declines. However, this does not seem to be the case with our patients, since our data indicate that the primary deficit concerns STM, rather than WM. 4. Conclusion In the present study, we tested three related hypotheses. 1st: That aphasic and memory deficits are due to a compromized common mechanism. 2nd: That this common mechanism concerns memory for verbal and spatial stimuli. 3rd: That this common mechanism is part of STM. We found that memory scores correlated with AS in both stimulus modalities, spatial and verbal. However, the correlation coefficients for STM and WM did not differ. Therefore, these data support the hypothesis of a common mechanism underlying aphasia and memory deficits (and not linguistic deficits only). Moreover, and with regard to our second hypothesis, the statistically significant correlations found for both verbal and spatial tasks, indicate that this mechanism should be stimulus modality-independent. Finally, regarding our third hypothesis, this
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