Brain Advance Access originally published online on July 22, 2003
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Brain, Vol. 126, No. 9, 1917-1934,
September 2003
© 2003 Guarantors of Brain
doi: 10.1093/brain/awg201
Working memory and executive functions in transient global amnesia
1 Inserm E0218-Université de Caen, Laboratoire de Neuropsychologie, CHU Côte de Nacre, Caen, 2 École Pratique des Hautes Études, CNRS 8581, Université René Descartes, Paris and 3 Service de Neurologie Vastel, CHU Côte de Nacre, Caen, France
Correspondence to: Professor Francis Eustache, Inserm E0218-Université de Caen, Laboratoire de Neuropsychologie, CHU Côte de Nacre,14033 Caen Cedex, France E-mail: neuropsycho{at}chu-caen.fr
Received November 21, 2002. Accepted April 20, 2003.
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Summary |
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Transient global amnesia (TGA) is usually considered to produce a profound impairment of long-term episodic memory, while at the same time sparing working memory. However, this neuropsychological dissociation has rarely been examined in detail. While a few studies have assessed some components of working memory in TGA, the results that have been obtained are far from conclusive. To clarify this issue, we carried out a comprehensive investigation of working memory in 10 patients during a TGA attack. In the first study, we report the results from three patients examined with a battery of neuropsychological tests designed to assess each of the three subcomponents of Baddeley’s model of working memory. In a second study, seven different patients underwent neuropsychological investigations that focused specifically on the central executive system, using a protocol derived from a study by Miyake and colleagues. Our findings showed that subcomponents of working memory, such as the phonological loop and visuo-spatial sketchpad, were spared in TGA patients. Specific executive functions that entailed inhibitory control, dual task performance, updating and shifting mechanisms were also found to be normal. However, we found significantly impaired performance for the Brown–Peterson test, and that TGA patients were significantly impaired in the recollection of their episodic memories. They also made reduced numbers of ‘remember’ compared with ‘know’ judgments in the episodic memory test several days after TGA. On the basis of our findings, it would appear that the episodic memory deficit during TGA is not related to elementary aspects of executive functioning. Our data also highlight the nature of the cognitive mechanisms involved in the Brown–Peterson task, which may well depend on long-term memory (such as the process of semantic encoding). Lastly, the selective deficit in recollective episodic memories observed in TGA may be principally related to medial temporal lobe abnormalities that have been reported in this syndrome.
Keywords: Brown–Peterson paradigm; encoding; episodic buffer; episodic memory; storage
Abbreviations: BEM = batterie d’efficience mnésique; C = chance; K = know; MQ = memory quotient; R = remember; R/K = remember–know; TGA = transient global amnesia; WCST = Wisconsin Card Sorting Test
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Introduction |
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Transient global amnesia (TGA) is a neurological syndrome occurring in middle age, with an aetiology that remains elusive. It is characterized by a profound, time-limited memory impairment of acute onset, without accompanying neurological deficits. Neuropsychological studies, performed during the acute phase, disclosed a disorder of episodic memory that results both in anterograde and retrograde amnesia. Analysis of some of the mechanisms involved in the anterograde amnesia show that TGA could be due to an encoding and/or a storage deficiency (Eustache et al., 1999
; Guillery et al., 2000, 2001, 2002). Other components of memory, such as procedural memory (Kazui et al., 1995; Eustache et al., 1997), priming effects (Kazui et al., 1995; Kapur et al., 1996; Eustache et al., 1997) and conceptual knowledge (Hodges, 1994; Kazui et al., 1996; Eustache et al., 1997, 1999) are preserved in TGA.
Few studies have evaluated working memory during the amnesic episode and the results, so far, are not conclusive. Most authors have assessed short-term retention with a forward digit span and a visuo-spatial span. According to Baddeley’s theoretical model of working memory, which describes two slave systems (Baddeley, 1986), the temporary storage and rehearsal of auditory-verbal information is subserved by the phonological loop while the visuo-spatial sketchpad performs a similar function for visuo-spatial information. Some authors suggest that a correct performance in the forward digit span argues in favour of a preservation of these slave systems (Goldenberg et al., 1991; Tanabe et al., 1991; Evans et al., 1993; Hodges, 1994; Härting and Markowitsch, 1996; Kazui et al., 1996; Eustache et al., 1997, 1999; Guillery et al., 2000).
Other tasks, such as the backward digit span, are used to assess the central executive. This third component is an attentional system involved in multiple cognitive processes and is responsible for the control of the two slave systems. An important characteristic of the central executive is its limited resources, which can be allocated to data processing and/or can be used to aid in storage in the slave systems. The results obtained when performing the backward digit span (a procedure that requires a reorganization of the information) during TGA are under debate. In most cases of TGA, patients’ performances in this task are within the normal range (Goldenberg et al., 1991; Tanabe et al., 1991; Evans et al., 1993; Hodges, 1994; Härting and Markowitsch, 1996; Kazui et al., 1996). However, Saito et al. (1997) reported pathological results in one patient when performing this task during the attack. Gallassi et al. (1986) also noticed the same pathological pattern in another patient, but this impairment persisted 1 month later. Such discrepancies could result from either the severity of the TGA, the stage when testing is carried out (acute phase or recovery phase) or from a real inter-individual heterogeneity. For instance, Eustache et al. (1999) reported two distinct episodic memory impairments (encoding or storage) in patients examined during the acute phase of TGA. Moreover, a neuroanatomical heterogeneity was evidenced following PET investigations, again made during the acute phase of TGA (Baron et al., 1994; Eustache et al., 1997; Guillery et al., 2002). In these latter studies, in which oxygen metabolism and cerebral blood flow were measured, the authors showed significant metabolic and haemodynamic changes in a number of brain regions (prefrontal cortex, amygdala and hippocampal regions).
Finally, as memory performances depend on the difficulty and the nature of the task, when the tasks used to assess the working memory become more complex, the performance appears to be more impaired (for a recent review see Brown, 1998). For example, Hodges and Ward (1989) used a verbal task in which five patients had to learn a list of six words during the acute phase of TGA. The results showed that the patients were able to repeat the whole list when recall was tested after 1 min. However, when the retention interval was filled by a distracting activity, the scores decreased considerably. Patients retained less than half of the items, whereas normal controls recalled all of the words. These results suggest an important susceptibility to interference during TGA. First, this finding could indicate a depletion of attentional resources. When patients are required to perform some distractor task, or to manipulate the information (e.g. reverse the sequence of digits), they do not have enough resources to both process and maintain the information. Secondly, these deficits could reflect a more specific disturbance of some executive process, such as the co-ordination of two tasks (i.e. to maintain and manipulate information).
Indeed, the central executive does not only correspond to a pool of resources, but it allows the selection, control and co-ordination of various processes. Baddeley distinguished a number of different functions associated with this system (viz. the capacity to inhibit irrelevant information, to selectively pay attention to relevant stimuli, to switch retrieval strategies, to activate information stored in long-term memory and to simultaneously execute two tasks) (Baddeley, 1996a, b, 1998). This theoretical conception of the central executive has been recently confirmed by the work of Miyake et al. (2000). These latter authors proved that different elementary executive functions can be fractionated.
Regarding the literature, executive functions in TGA have been the subject of few investigations and the results remain inconclusive. Inhibition, as assessed by the Stroop task, appears preserved in four patients tested during the acute phase (Regard and Landis, 1984; Hodges, 1994), whereas Stillhard et al. (1990) revealed an impairment of inhibition processes in one patient tested 15 h after the beginning of the episode. Goldenberg (1995) explored, in one patient, the ability to shift between mental sets with a task derived from the Wisconsin Card Sorting Test (WCST; Berg, 1948; Grant and Berg, 1948). The patient was examined during TGA and pathological scores were obtained, although the patient’s scores were not analysed statistically. Moreover, the WCST appears to be related strongly to the shifting and inhibition functions (Miyake et al., 2000). By employing the Trail Making Test of Reitan, Hodges assessed the mental set-shifting ability of two patients during the acute phase of TGA (Reitan, 1958; Hodges, 1994). He compared the patients’ results obtained during TGA with those obtained the next day and concluded that these abilities were preserved during the attack. Categorical and orthographical fluency tasks have also been performed in several studies. Such tasks are usually used to explore the implementation of retrieval strategies from long-term semantic memory. In these tasks, two typical disturbances have been described in conditions of TGA. First, patients produce many perseverative errors, which could result from the massive anterograde amnesia (Hodges, 1994; Eustache et al., 1999). Secondly, the number of correct responses can be significantly decreased. A low correct response score has been interpreted as reflecting an impaired strategy of retrieval from long-term memory, since the other tasks argue in favour of preserved conceptual knowledge of semantic memory (Eustache et al., 1997).
In conclusion, the foregoing data should suffice to show that the neuropsychological pattern of the executive functions during TGA is still under debate. Indeed, no study has extensively assessed the central executive in the light of a model of working memory. For this reason, we investigated working memory during the acute phase of TGA by means of a prospective protocol, which allowed us to explore the phonological loop, the visuo-spatial sketchpad and the central executive. This investigation was designed to state explicitly which system is disturbed in TGA and whether working memory impairment could contribute to the episodic memory deficits, especially during the encoding phase. In order to specify these theoretical issues, two studies were undertaken. The first study, on the basis of Baddeley’s tripartite model (Baddeley, 1986), assessed each of the three subcomponents of the working memory in three patients. The second study (largely inspired by the recent report of Miyake et al., 2000), focused on the central executive. In the second study we tested, in seven other patients, each elementary function (shifting, updating and inhibition) as proposed by these authors. The 10 patients gave their consent to the study after detailed information was provided to them and the study was performed in accordance with the Declaration of Helsinki. Approval was given by the University of Caen.
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First study |
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Methods
We evaluated three TGA patients with a prospective protocol to assess general cognitive functions, episodic memory and working memory. This neuropsychological protocol, specially designed for this study, was modular and could be applied to the patients in the form of short sequences interleaved with medical examinations.
The general cognitive assessment included subtests of spatio-temporal orientation (Mattis, 1976) and visuo-constructive abilities (Signoret et al., 1989). General knowledge was assessed by means of a matching figures task (according to a common perceptive criterion), a semantic categorization task and a categorical fluency task (taken from the Mattis Dementia Rating Scale; Mattis, 1976). The control group consisted of 10 age-matched subjects (mean age 64.5 years, SD 5.2).
The episodic memory task was derived from Grober and Buschke’s procedure (Grober and Buschke, 1987) and has been used in other studies of TGA (Eustache et al., 1999; Guillery et al., 2000, 2001, 2002). This task was aimed at differentiating between selective disorders of encoding, storage and retrieval of information in episodic memory (for details and normative data see Eustache et al., 1999). The task consists of one list of 16 words belonging to 16 different semantic categories. First, the subject was asked to process each word in depth by generating a sentence containing the word (for example ‘turnip’). Then, in order to ensure the actual carrying out of deep encoding, a task of immediate cued recall was given after every two words by providing the appropriate semantic category (‘what was the vegetable?’). In the instance of failure, a second processing and immediate cued recall was made. This procedure was repeated until the correct recall of the word was achieved. This phase involves several cognitive processes. Patients had to retrieve knowledge from semantic memory in relation to the target word. They had to maintain and manipulate this knowledge in working memory in order to generate an adequate sentence. Finally, they had to conserve the first target word in working memory for a few seconds while they process the second target word of the pair. Hence, two memory systems are implicated in this procedure: semantic memory and working memory. Immediately after processing the 16 words, retrieval was assessed through both free recall and recognition. This test produced three scores, namely immediate cued recall, free recall and recognition scores. The analysis of the score profiles makes it possible to infer the nature of the disturbance responsible for the anterograde amnesia. Thus, in the case of a presumed encoding disturbance, patients would not be able to recall the target words upon immediate cued recall. In the case of a presumed storage disruption, despite adequate processing, performance in free recall and recognition would be pathological. Finally, performance that is significantly better in recognition than in free recall would reflect a preferential retrieval disorder since the patient benefits from the visual presentation of the target item.
The working memory assessment comprised five tasks used to explore the three components of Baddeley’s theoretical framework. The phonological loop was tested by a forward digit span (for normative data see Grégoire and Van der Linden, 1997) and the visuo-spatial sketchpad was assessed by a forward visuo-spatial span (Signoret, 1991; and for normative data see Eustache et al., 1995). Three other tasks to assess the central executive were given to the patients. We used a backward digit span (for normative data see Grégoire and Van der Linden, 1997), an updating task and Brown–Peterson’s paradigm (Brown, 1958; Peterson and Peterson, 1959). The updating task is derived from the N-Back task and consists of a string of 30 letters sequentially presented in an oral manner. The subject had to evaluate whether each letter added was the same as any one of the preceding three letters. The score obtained in this task corresponded to the number of recognized letters. The patient’s scores were compared with those of a group of 17 subjects aged between 60 and 79 years (mean age 66.8 years, SD 5.2). In the Brown–Peterson paradigm, the subject had to memorize three short words (written on an index card) for a variable delay with inclusion of an interfering task. After reading the three words, the subject was asked to recall immediately the items (delay of 0 s) or to count audibly backwards from a given number, one by one for either 3, 6, 9 or 18 s, before recalling the words. The rate of digit production was not strictly monitored, but subjects were encouraged to count as quickly as possible (at a rate of approximately two to three numbers per second) and were cautioned when the regularity of the rate of counting became too slow. The 0, 3, 6, 9 and 18 s delays occurred five times during the test and were equally distributed in five blocks. The ordering of each trial into the blocks was randomized. For each delay, the percentages of correct responses, omissions and intrusions were calculated. For this task, the control group consisted of 10 age-matched subjects (mean age 64.5 years, SD 5.2).
Each patient was studied first during the acute stage of TGA and a second time the next day. During the third examination (
1 month later), all these tests, except the episodic memory task, were repeated. In order to assess general memory performance, we used the Wechsler Memory Scale (Wechsler, 1969) during the second examination and the ‘batterie d’efficience mnésique’ (BEM 144; Signoret, 1991) during the third examination.
Results
Patients
Patient AL is a 68-year-old right-handed woman, retired cook with a history of arterial hypertension treated with beta-blockers and diuretics. On the September 2, 2000, at around 10:00 a.m., AL was at home when she was informed of her daughter’s breast cancer. Two hours after this phone call, AL started repetitive questioning about her daughter. Her husband noticed that she did not remember the phone conversation, but seemed nevertheless worried. When she arrived at the University Hospital of Caen at around 1:00 p.m., the neurological examination was normal except for the memory disturbance. The anterograde amnesia was massive and the retrograde amnesia covered at least the previous week. The EEG was normal. The neuropsychological examination began at around 5:00 p.m., when the patient was still in the acute phase. Two hours after the end of the examination, AL began to recover. The TGA appears to have lasted about 7 h. The next day, AL had no memory disturbance other than lacunar amnesia concerning the period of the TGA and the few minutes before. The results for the memory tests carried out the next day, and roughly 1 month later, were also normal: she obtained a MQ of 116 on the Wechsler Memory Scale and the global memory score assessed with the BEM was 63.5 (controls mean 58.2, SD 7.9). A brain CT scan made a few days later was normal.
Two other patients, 66 (OLN) and 69 (NB) year-old women, underwent testing during their TGA. They fulfilled the operational criteria for TGA according to Hodges and Warlow (1990), and they had no previous medical history. The TGA attacks varied from 6 to 7 h in duration. Both patients were studied in the early recovery phase about 4 h after the start of the episode. At this time, both patients still had an anterograde and a retrograde amnesia accompanied by repetitive questioning but without neurological deficits. Preceding the TGA, precipitating physical factors had been noted (one woman had been taking a shower and the other doing some domestic paintwork). The next day, neither of them had any memory disturbance other than lacunar amnesia concerning the duration of the attack. The results for the memory tests carried out the next day, and roughly 1 month later, were normal: patients OLN and NB obtained MQs of 112 and 129, respectively, on the Wechsler Memory Scale, and the global mnesic score assessed with the BEM was 57 for OLN and 67.5 for NB (controls mean 58.2, SD 7.9). Diagnostic investigations made during the TGA episode for NB (EEG, brain CT scan) and the next day for OLN (EEG, brain CT scan, Doppler examination of the supra-aortic vessels) were normal.
Neuropsychological scores during TGA
The scores for the battery of neuropsychological tests during TGA are reported in Table 1 and show that orientation in time was significantly disturbed for the three patients. Visuo-spatial constructive abilities were preserved except in one patient (AL), who did not copy correctly the geometrical figures and obtained a score of 10 out of 12. Performance on the semantic categorization and the figures matching tasks were normal, or in the low normal range. In the verbal fluency task, all three patients had normal performance but produced several perseverative errors.
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(raw scores with corresponding Z scores): first study
For the episodic memory test, all three patients could make a sentence with the target word. However, for two patients (AL, NB) the number of correct responses in the immediate cued recall, the free recall and the recognition tasks was significantly low. The performance of patient OLN was significantly impaired in both free recall and recognition, a finding that is in contrast to her normal score in the immediate cued recall task.
In the working memory tests (forward digit and visuo-spatial spans), the performance of the three patients was in the normal range. They also carried out the backward digit span and the updating task correctly. Results using the Brown–Peterson paradigm (Table 2) showed that, apart from the immediate recall (delay 0 s), patients’ scores were significantly decreased when a delay of 3 or 6 s was employed in the test. Indeed, for two patients (AL and NB) the percentage of correct responses during TGA was pathological over the whole test interval (3, 6, 9 and 18 s delays). Omissions and perseverative errors were more numerous than in control subjects. AL produced 23 perseverations [for example, the word ‘bois’ (wood) was repeated five times, ‘nez’ (nose) four times, ‘gare’ (station) and ‘pont’ (bridge) three times each] and patient NB produced six perseverations [the word ‘age’ (age) was repeated three times, ‘bois’ twice and ‘soir’ (evening) once]. The third patient’s (OLN) scores were less impaired than the two others during the attack, since the percentage of correct responses was in the normal range for the 9 and 18 s retention interval. This patient produced 20 perseverations [for example, the word ‘bois’ was repeated eight times, ‘sac’ (bag) three times, and ‘peau’ (skin) and ‘base’ (base) twice each], but contrary to the two others, she made few omissions (the percentage of omissions was in the normal range for all the delays).
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Neuropsychological scores the day after the TGA and at follow-up
Table 1 shows the results of the three patients for the battery of neuropsychological tests carried out the following day and roughly 1 month later. In both cases, general cognitive functions were preserved for the three patients.
The day after TGA, two patients (AL and OLN) performed normally on the episodic memory test, whereas immediate cued recall of the third patient (NB) was still slightly impaired (14 out of 16).
The day after TGA and at follow up, the results of the Brown–Peterson paradigm returned to normal for two patients (OLN, NB; Table 2). The third patient had improved her performance but not enough to be in the normal range.
Discussion of the first study
The main objective of this study was to investigate working memory in TGA by means of a prospective protocol that allowed us to assess each of the three components of Baddeley’s model, namely the phonological loop, the visuo-spatial sketchpad and the central executive. The second aim was to describe the relationship between working memory performance and the episodic memory impairment that is characteristic of this pathology. This study reports three patients fulfilling the operational criteria for TGA of Hodges and Warlow (1990), examined in the acute stage, the next day and roughly 1 month later with a neuropsychological protocol comprising a working memory and an episodic memory assessment. In the case of the working memory tests, the patients correctly performed the forward digit and visuo-spatial span tasks. These findings suggest that patients were able to mobilize the two slave systems to recall a limited amount of information (verbal or visuo-spatial). Assessment of the central executive revealed a divergence between the three tasks used. Indeed, the patients’ normal ability to perform the backward digit span and the updating task stands in contrast with the pathological scores obtained in Brown–Peterson’s paradigm. Performance in this latter task was significantly impaired during TGA (after 3, 6, 9 or 18 s delay) for all patients, and was still pathological the next day, and 1 month later, for one of them. This divergence probably results from the specificity of the processes involved in each of these three tasks. The backward digit span involves both the phonological loop (to actively store the digits) and the central executive’s ability to reorganize the material (Belleville et al., 1998). Our updating task, derived from the N-Back span, requires patients to store the three consonants read by the examiner and to make a ‘yes/no’ recognition for each added letter. In this task, the patients have to continuously modify the content of working memory according to new incoming information (i.e. discard old consonants while new ones are registered). The updating task requires several cognitive processes (i.e. encoding, temporary maintenance and rehearsal, tracking of serial order, updating and matching, and response processes). However, we used a simplified version of the N-Back test, which may not involve such processes. Indeed, the patients’ correct performances in our updating task would be principally supported by a feeling of familiarity during the matching stage.
The Brown–Peterson paradigm may be dissociated from other measures of working memory since it involves several components of working memory. First, this paradigm was specifically designed to test the short-term retention of verbal material in the presence of an interference task. This task requires the patients’ ability to store three words during a short delay with the interval filled by a distractor activity which consists of counting backwards. Baddeley (1971) noticed two processes of ‘forgetting’ in the Brown–Peterson task. The first process is direct and occurs just after the presentation of the items within a 5 s delay, it depends on a ‘primary’ memory component (corresponding to the phonological store in the current model of working memory) and could correspond to a rapid trace decay. The second refers to an indirect mechanism, observed after 5 s, and is the consequence of a proactive-interference action. This mechanism of competition from earlier items could be better regarded as a phenomenon of long-term memory rather than of short-term memory (Baddeley, 1997). Thus, according to Baddeley, two different types of encoding lead to different representations in two different systems of memory: a phonological encoding in working memory and a semantic encoding representation in long-term memory (Baddeley, 1986). In the phonological process, material is preferentially encoded along a phonological dimension through the phonological loop and the recall of items is affected by the phonological similarity. Baddeley et al. (1984) explored the influence of articulatory suppression on immediate memory for auditorily presented items and showed that the phonological similarity effect is not completely abolished by articulatory suppression. Semantic encoding refers to a deeper processing on the semantic properties of the items and allows the elaboration of a more stable memory trace transferred in long-term memory. Studies in the Korsakoff syndrome are in accordance with this hypothesis. Cermak et al. (1973) provided lists of nine words belonging to three different semantic categories. Korsakoff patients were either informed of the organization of the list or not. Results showed that the immediate recall in response to categorical cues was not improved when patients were instructed that the words belonged to categories. The authors concluded that the patients’ deficit could be related to a spontaneous phonological encoding rather than semantic encoding. This tendency to encode acoustically in working memory, rather than semantically in long-term memory, could result in an important number of acoustic errors (Brooks and Baddeley, 1976). Our findings fit well with the data reported by Cermak et al. (1973). The nature of perseverative errors noted with our patients [e.g. when considered acoustically, ‘nez (ne)’ for ‘pied (pje)’, ‘bois (bwa)’ for ‘loi (lwa)’, ‘joie (zwa)’ for ‘roi (rwa)’], could likewise suggest a tendency for our patients to spontaneously encode the items on an acoustic level in working memory rather than on a semantic level in long-term memory and could thus contribute to the greater occurrence of phonological confusions. In their study, Sebastian et al. (2001) examined the results of 40 Alzheimer’s disease patients in a Brown–Peterson task and made a qualitative analysis of the errors. The categorization of errors showed that the patients had a larger number of phonological confusions and perseverations. First, the authors suggested that the phonological errors seem to indicate the predominance of a phonological encoding. The findings of our study appeared to support this hypothesis. However, the authors also observed high rates of perseverations and concluded that the patients were unable to update the contents of their working memory. According to this hypothesis, our results, in which perseverations were noted, could also indicate an impairment of the updating function, thus prompting us to further test this executive function with a more appropriate task. These perseverative errors could also reflect a deficit in the inhibition of the irrelevant information. In fact, Warrington and Weiskrantz (1971) suggested that impairment observed in the amnesic syndrome could result from a failure to inhibit, or dissipate, stored information. With the Brown–Peterson paradigm, Cermak and Butters (1972) demonstrated that the performance of the Korsakoff patients increased when the time interval between each trial was increased (1 min between trials), and suggested that the patients showed an important sensitivity to proactive interference, i.e. they were less able to resist and to inhibit information that was previously relevant to the task, but had since become irrelevant (Dempster and Cooney, 1982). Thus, failure to inhibit previously acquired information could account for the pattern of results reported in the present study, and the perseverative errors observed in the fluency task would tend to reinforce this hypothesis. According to the interference hypothesis, we should observe an increase of the perseverations over the number of trials (Keppel and Underwood, 1962). However, in the present study, a detailed analysis of the results did not reveal this pattern. The number of correct responses, omissions and perseverations were equally distributed among the five time-blocks of the task. These results allow us to adjust the hypothesis of an excessive susceptibility to proactive interference during TGA.
Some authors evoked other executive functions which may be involved in the Brown–Peterson paradigm, such as a divided attention capacity (Morris, 1992; Collette et al., 1999) and ‘switching’ (i.e. the ability to switch from the distractor activity to the retrieval of the target information; Leng and Parking, 1989). It becomes more apparent that the Brown–Peterson paradigm is a complex task which involves various cognitive processes: encoding in long-term strategies, several executive processes such as updating, inhibition of interference, divided attention and shifting. Nonetheless, our study does not allow us to specify exactly the processes responsible for the deficit in the Brown–Peterson paradigm and to do so would require further investigations.
In the case of episodic memory, the results illustrate two profiles of impairment in this task. The first impairment (observed in one patient) shows pathological performances in free recall and recognition tasks, which is indicative of a storage disturbance. The second impairment (observed in two patients) is characterized by pathological performances of immediate cued recall, free recall and recognition. This pattern of performance suggests an inadequate initial processing of material to-be-remembered and thus could reflect an encoding deficit. This double profile is in keeping with the results already reported by Eustache et al. (1999). Of the three patients, two, who were examined during the early recovery phase, demonstrated an opposite pattern of impairment. Thus, in this case, the discrepancy appears less likely to be related to the stage at which the test was carried out, but rather from differences arising from intersubject variability. These severe episodic memory deficits can explain the numerous perseverative errors in the verbal fluency task due to the progressive forgetting of the answers produced (Hodges, 1994; Eustache et al., 1999).
In conclusion, the results of this study suggest preservation of the phonological loop and of the visuo-spatial sketchpad during TGA. Furthermore, they show that the patients’ ability to manipulate the information remains intact. These data also argue in favour of a preserved updating capacity, an issue never previously assessed in this pathology. However, it seems relevant to confirm this latter result with a more sensitive task, since the modified version of the N-Back test could be supported only by a feeling of familiarity. Moreover, deficits observed in the Brown–Peterson paradigm could reflect a specific impairment of some executive process, an inability to update the contents of working memory, to divide, to shift attention or maybe to inhibit the interferences. These deficits could also stem from an inability to spontaneously encode items on a semantic level (i.e. mechanisms involving long-term memory). The results of this study argue in favour of deficits that affect the executive functions involved in Brown–Peterson’s paradigm and episodic memory. However, it seems premature to conclude that a ‘direct link’ exists between the executive functions deficits and episodic memory impairment in TGA. The next study extends further our first results by taking a more in-depth approach and completes the working memory examination with a more sophisticated investigation of the executive functions in reference to Miyake’s study (Miyake et al., 2000).
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Second study |
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TopSummaryIntroductionFirst studySecond studyDiscussionReferences |
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Methods
The neuropsychological protocol of this study was specially designed to investigate the central executive. It also included a general cognitive and an episodic memory assessment. Seven new patients underwent neuropsychological tests during TGA, the next day and about 1 month later.
The general cognitive assessment consisted of the same tasks as those used in the first study (spatio-temporal orientation, visuo-constructive abilities and general knowledge).
Episodic memory was evaluated using the task which has been already described in detail (vide supra). However in this instance, taking into account recent developments in the study of episodic memory, we included within the task a remember–know (R/K) paradigm that allows one to assess the subjective experience accompanying the retrieval. ‘Remember’ (R) responses refer to the autonoetic consciousness that allows us to be aware of subjective time in which events happened (Tulving, 1985, 2002). ‘Know’ (K) responses are based on a feeling of familiarity and are an indication of the noetic consciousness that characterizes the semantic memory (Gardiner, 1988, 2001; Gardiner et al., 1998). During the recognition task, the subject has to indicate his/her conscious subjective experience accompanying the retrieval. The patient gives either an R response, if retrieval is accompanied by recollection of the context as a re-experiencing of the information from the learning context (i.e. thoughts, feelings or perceptions), or a K response, if retrieval is achieved without such recollection. In addition, a ‘chance’ (C) response gives the opportunity for the patient to indicate that he/she is not sure of the response (Gardiner and Conway, 1999). Upon recognition of the correct word among the three distractor items, the patient was instructed to say precisely whether such recognition was associated with details about the first presentation. Three replies were possible: first, he remembered the word because he could detail the associations he had made and the sentence he had generated during the encoding phase (R); secondly, he recognized the word on the basis of a feeling of familiarity but without further recollection about his thoughts (K); thirdly, he was unsure of why he chose this word (C). A parallel form of this test was conducted 1 month after the TGA episode.
Working memory was investigated by means of tasks that assessed the phonological loop, the visuo-spatial sketchpad, and several executive functions. As in the first study, the phonological loop and the visuo-spatial sketchpad were tested with the forward digit and visuo-spatial spans, respectively (Wechsler, 1991). Various executive functions attributed to the central executive have been previously investigated and documented by Baddeley (1996a). The first function concerns the ‘manipulation of information’, and can be defined as the process of actively and consciously modifying the format of the information to-be-recalled (Belleville et al., 1998). Therefore, we used both backward digit and visuo-spatial spans (Wechsler, 1991), which involved verbal and visuo-spatial material manipulation, respectively. Different functions, more or less complex, have been attributed to the central executive. In a recent study, Miyake et al. (2000) provided arguments in favour of distinguishing between three elementary executive functions, namely a ‘shifting’ process, an ‘inhibition’ of inappropriate responses and an ‘updating’ function. In the case of this study, we investigated these functions by employing the Trail Making Test (parts A and B), the Stroop test and the running span task, respectively. The Trail Making Test requires rapid shifts between two sets of stimuli (letters and digits) (Reitan, 1958). For this task, we considered both performance with respect to time and the number of errors produced. For the Stroop test (Stroop, 1935), which aims to assess the patients’ ability to inhibit the inappropriate response, we calculated an interference coefficient. To achieve this, we subtracted the predicted score (calculated from the results in the first and second conditions of this task: word and colour conditions) from the results obtained in the third part of the test (interference condition). The running span task has been developed in our laboratory following on from the work of Van der Linden et al. (1999). Strings of consonants of variable length (4, 6, 8 or 10 letters) are given orally without giving prior knowledge of the length of the consonant string, and patients are required to recall serially the four most recent items (Pollack et al., 1959). This task comprises 16 strings of consonants and, as such, the patients can obtain a maximal score of 16. Finally, we used a dual-task paradigm to investigate the multi-tasking component of working memory considered by Baddeley, to be a primary function of the central executive (Baddeley et al., 1997). Patients were instructed to perform in 2 min, two simultaneous tasks: a motor tracking task, that relies on the visuo-spatial sketchpad, with the concurrent requirement to hear and repeat back sequences of digits involving the phonological loop. In the tracking task, subjects were required to cross out boxes (size 1 cm square) that had been linked to form a path. For the memory span task and the tracking task, the measure of performance was taken as the proportion of digit lists correctly recalled and the number of boxes successfully marked, respectively. For each patient, we also calculated a dual task score which took into account their results in both tasks independently. The score was calculated as [1 – (pm + pt)/2)] x 100, where the value ‘pm’ corresponds to the proportional decrease of memory performance during the dual task and ‘pt’ to the proportional loss of tracking performance (for more details see Baddeley et al., 1997).
The control group for the whole protocol consisted of 20 subjects aged between 45 and 75 years (mean 60.5 years, SD 9.1). This group was divided into two subgroups of 10 age-matched subjects (45–60 and 61–75 years).
Results
Patients
Table 3 summarizes the clinical data for the seven patients, who presented with an episode of TGA. All patients, aged between 55 and 75 years, fulfilled the criteria of TGA (Hodges and Warlow, 1990). In five of the patients, physical precipitating events were known to precede the TGA (e.g. strenuous physical activity, taking a shower). In the two others, the attack had occurred after psychological precipitating events (emotional stress). When the patients arrived at the University Hospital of Caen, neurological examinations were found to be normal except for the memory disturbance and the disorientation in time. The neuropsychological examination was performed between 2 and 7 h after the onset of the episode; four patients were examined during the acute phase, and three others patients were studied in the early recovery phase. During the recovery phase, the patients produced less C responses in the episodic memory task than those examined in the acute phase. Moreover, the clinical signs (repetitive questioning, disorientation and amnesia) were less dramatic during the recovery phase. The duration of TGA ranged from 5 to 12 h. The next day, patients had no memory disturbance other than lacunar amnesia concerning the duration of the attack. Results for the diagnostic investigations are reported in Table 3.
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Neuropsychological results during TGA
Table 4 gives the patients’ scores for the battery of neuropsychological tests during the attack. Orientation in time was significantly disturbed in all seven patients. In the case of geometric figures, designed to assess the visuo-constructive abilities, all patients performed normally. Conceptual knowledge was also normal. On a verbal fluency task, six patients produced significantly more perseverations than the controls—a finding that could result from their memory deficit. In addition, one patient obtained a pathological score for the number of correct responses in this verbal fluency task. Such a result, previously reported in the literature, has been interpreted as reflecting an impaired strategy of retrieval from semantic memory (Eustache et al., 1997
).
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In four patients, the results obtained in the episodic memory test would argue in favour of an encoding deficit. Indeed, patients AB, JG, SV and LB obtained a pathological score in immediate cued recall, free recall and recognition tasks. For the three other patients (YY, JA and BS), free recall and recognition scores were significantly impaired but no major difficulty was noticed in the immediate cued recall task. This finding suggests the involvement of a storage deficit for these latter three patients.
During the TGA episode, patients’ responses in the R/K paradigm were dramatically different from those of the control subjects. One patient produced an R response and three K responses, and two other patients produced six K responses each. Except for these specific cases, correct performances in the recognition task were associated with a C judgement.
Examination of working memory during TGA revealed normal scores in the verbal and visuo-spatial spans for the seven patients. The five other tasks used to assess the elementary executive functions, namely the manipulation, shifting, inhibition, updating and co-ordination tasks, were all performed correctly. Only one patient obtained a significantly reduced score in the backward visuo-spatial span.
Neuropsychological results the day after TGA and at follow-up
The day after the TGA (Table 5), three patients still had a reduced score in the time orientation test. Patient YY did not remember the Prime Minister’s name, JG did not remember the mayor’s name, while SV and BS could not recall the correct date. Nonetheless, the episodic memory results were back to normal overall. However, one patient produced significantly less R responses and more K responses than the controls. Performances in the working memory tasks were in the normal range for all the patients. One month later (Table 6), only one patient still had a reduced score in the time orientation test and one other patient in the semantic categorization task. This latter patient had also a pathological score in the number of R responses.
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Discussion of the second study
The main objective of this second study was to investigate the subcomponents of working memory as defined by Baddeley (1986)
and elementary executive functions as described by Miyake et al. (2000). A second aim was to establish the relationship between working memory and performance on the episodic memory task (which showed a encoding deficit in four patients and a storage deficit in three others), in accordance with recent theoretical formulation of episodic memory (Tulving, 2001, 2002). This prospective study of working memory, carried out with seven patients, allowed us to clarify the state of this system during the acute phase of TGA. By means of an original protocol, the results of this study support preservation of executive functions. The ability to manipulate information, to shift between mental sets and to inhibit irrelevant information as assessed by the backward digit and visuo-spatial spans, the Trail Making Test and the Stroop task, respectively, all seems to remain intact. Moreover, this study demonstrates (by means of tests never before employed in TGA), that patients can correctly co-ordinate various items of information while their attention is divided (as in the dual-task paradigm). Their ability to update information is also preserved. Our overall results support a preservation of the various components of working memory, despite the fact that one patient showed a slight impairment in the backward visuo-spatial span. As Brown (1998) reported, such an impairment in the performance of tasks requiring spatial abilities could appear during the acute phase of TGA. Results for the R/K paradigm observed during TGA, and never before reported in this pathology, illustrate clearly the severity of the anterograde amnesia and confirm the dramatic episodic memory impairment as noted with this appropriate methodology. Our original paradigm also highlights persistent impairment of episodic memory after the TGA episode. Indeed, most of the patients produced less strictly episodic recollections than the control subjects. Thus, the results suggest either an incomplete recovery the next day as well as roughly 1 month later (Hodges and Oxbury, 1990), or a persistent memory impairment in episodic memory following TGA. It is noteworthy that the high sensitivity of the R/K paradigm allows one to demonstrate long-term subclinical disorders in TGA. Thus, the recent data in functional imaging that show an increased activity in the hippocampus occurring during R responses (Eldridge et al., 2000) and the dysfunction of the medial temporal structures that have been reported during the acute stage of TGA (Warren et al., 2000; Guillery et al., 2002), could support the hypothesis that the persistent deficit in recollective judgments may be related to prolonged medial temporal lobe abnormalities (Kessler et al., 2001). In conclusion, this study reports original results on working memory collected during the acute phase of TGA by means of tasks (most of which were employed for the first time) especially designed to isolate various executive functions. The data demonstrate the integrity of these executive functions in contrast with the presence of a profound episodic memory impairment. This unexpected pattern consequently suggests that the major deficits of episodic memory observed in TGA are not directly related to the executive processes.
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Discussion |
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TopSummaryIntroductionFirst studySecond studyDiscussionReferences |
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According to current theoretical models (Baddeley, 1986
; Miyake et al., 2000), the results of the two present studies suggest a preservation of executive functions in seven patients examined during the acute phase of TGA (see Fig. 1). However, in the first study, the three patients performed poorly at the Brown–Peterson task. Pathological scores in this sensitive task could result from an impairment of executive functions focused on divided attention, inhibition, shifting and updating processes (i.e. the four processes implicated in the Brown–Peterson task; Leng and Parking, 1989; Binetti et al., 1995; Collette et al., 1999; Sebastian et al., 2001), or from an impairment of mechanisms operating in long-term memory. The results observed in the second study clearly invalidate the executive hypothesis. Related to our findings, Giovagnoli et al. (1996) investigated interference effects in lateralized temporal lobe epilepsy with a task derived from the Brown–Peterson paradigm and showed that the impaired performance was correlated with the severity of learning, but not with deficits on executive tasks (word fluency test and WCST). Consequently, as Baddeley suggests (Baddeley, 1997), memory processes involved in the Brown–Peterson task may be more akin to long-term memory mechanisms. In fact, deficits in the Brown–Peterson paradigm may result from an inadequate semantic encoding in long-term memory. A processing occurring only in working memory and based on the superficial characteristics of the material, such as the phonological or acoustic features, could be responsible for the decreased recall performance and increased phonological perseverative errors in the Brown–Peterson task (Stage 1 in Fig. 1).
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The episodic memory investigation, performed by means of an original task and in agreement with current definition of episodic memory as proposed by Tulving (Tulving, 2001
, 2002), has demonstrated encoding and/or storage disorders and a major perturbation of recollective judgments. The continuing impairment of autonoetic consciousness after TGA may be largely related to minimal medial temporal lobe damage.
In the first stage of the episodic memory task, the deep processing required for sentence generation was, in some patients, performed correctly (as confirmed by the immediate cued recall of the words) and should compensate for the spontaneous encoding deficit. However, some patients still had pathological performances on the immediate cued recall task, an observation that suggests the involvement of an additional impairment that could occur after the semantic processing. The generation of a correct sentence requires association of the target word with long-term semantic knowledge. This operation results in a specific episodic memory trace. Baddeley recently theorized this phenomenon (Baddeley, 2000, 2001) and proposed a fourth component to the model of working memory: the ‘episodic buffer’, which would correspond to a limited-capacity temporary storage system that is capable of integrating information from a range of sources into a single complex structure or episode. The episodic buffer acts as an intermediary between the subsystems (the slave systems and long-term memory), which use different codes, binding them into a unitary multi-dimensional representation (Baddeley and Wilson, 2002). The episodic buffer is also assumed to use representations in long-term memory and combine them into novel episodes. It is capable of maintaining, in a temporary manner, the episode that will be transferred to long-term memory. If such a concept were to hold true, then the ability to maintain two sentences in two distinct episodes (in order to perform the immediate cued recall task), could be dependent of the integrity of the episodic buffer. The results of our study support the view that, even if the semantic encoding is required, the pathological performances obtained in the immediate cued recall (which were noted in some patients), could have been caused by a disturbance of the episodic buffer (Stage 2 in Fig. 1). For the other patients, who could correctly perform semantic encoding, the normal scores obtained in the immediate cued recall are evidence in favour of a preservation of the episodic buffer. In such a case, the episodic memory impairment could rather depend on a long-term storage deficit, as shown by the pathological scores in the free recall and recognition tasks (Stage 3 in Fig. 1).
In conclusion, this study confirms that either the encoding or storage components, or both, of episodic memory may be impaired in TGA. Moreover, the extensive working memory investigation, carried out for the first time in the acute phase of TGA, has shown that the slave systems and the executive functions were spared. However, it would be interesting to extend the investigations of the phonological loop and the visuo-spatial sketchpad by using specific tasks to dissociate the storage and rehearsal processes. We thus suggest that an inability to use spontaneously the appropriate strategies of semantic encoding in long-term memory could result in pathological performances in the Brown–Peterson paradigm. One could speculate that in some of our patients, an impairment of the episodic buffer (as defined by Baddeley) could be responsible for the disruption of an efficient transfer of multimodal information in episodic memory. In the other patients, the four subcomponents of the working memory (including the episodic buffer) remained relatively intact. In this case, TGA would be restricted to an impairment of the storage processes in episodic memory.
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Acknowledgements |
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The authors wish to thank Dr Alan Young for reviewing the English in this manuscript, Stephanie Lecornu and Caroline Urban for their help in the neuropsychological examination of the patients, and the two anonymous referees for their helpful comments.
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References |
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