Cognitive Procedural Learning in Amnesia

BRAIN AND COGNITION ARTICLE NO.

32, 441–467 (1996)

0076

Cognitive Procedural Learning in Amnesia KLAUS SCHMIDTKE, RENE´ HANDSCHU, AND HEIKE VOLLMER Neurological Clinic and Research Program in Neuropsychology and Neurolinguistics, University of Freiburg, Germany This group study examined the role of residual declarative memory and taskspecific cognitive abilities for cognitive procedural learning in amnesia. 20 amnesic patients and 40 control subjects were studied, using four new cognitive tasks, as well as the Tower of Hanoi and a Mirror Reading task. On the cognitive tasks, but not on Mirror Reading, the learning of amnesic patients was significantly impaired relative to controls. Between- and within-group differences in learning were found to be statistically related to cognitive abilities that are involved in the processing of the procedural tasks. In amnesic patients, significant effects of residual declarative memory on learning scores were not observed, but there was indirect evidence for a role of memory in two tasks. The analysis of the correlative relationship between absolute procedural task performances and cognitive abilities indicated a prolonged dependence on nonspecific intellectual abilities in amnesic patients, suggesting a retarded transition to more advanced stages of skill acquisition.  1996 Academic Press, Inc.

INTRODUCTION

Procedural learning, or skill learning, refers to improvement in skills through practice. Together with priming, classical conditioning, habituation, adaptation-level effects and emotional learning, procedural learning forms a heterogeneous class of ‘‘implicit’’ memory phenomena (Roediger, 1990; Schacter, 1992; Schacter et al., 1993). Implicit learning is independent of conscious awareness and recollection, and can only be shown by demonstration. Various types of implicit memory were found to be preserved in amnesic patients (Brooks & Baddeley, 1976; Cohen & Squire, 1980; Kapur, 1988). Explicit or declarative memory, on the other hand, refers to the storing and handling of factual knowledge. While procedural learning may be subdivided into motor, perceptual, and cognitive skill learning, any given task can involve more than one type of Address correspondence and reprint requests to Dr. K. Schmidtke, Neurologische Universita¨tsklinik, Breisacher Strasse 64, 79106 Freiburg, Germany. 441 0278-2626/96 $18.00 Copyright  1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

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processing. Examples of cognitive tasks include computer programming and data entry (Glisky et al., 1986; Glisky & Schacter, 1987, 1989; Glisky, 1992), learning of mathematical rules (Wood et al, 1982; Charness et al., 1988; Milberg et al., 1988), and the Tower of Hanoi task (Cohen, 1984). A further type of procedural task is the serial reaction time paradigm (Nissen & Bullemer, 1987; Nissen et al., 1989). Dissociations in the learning of different skills support the view that procedural learning is itself a heterogeneous phenomenon (Brooks & Baddeley, 1976; Beatty et al., 1987; Harrington et al., 1990). The neuronal mechanisms that underlie procedural learning are unclear. Findings in patients with basal ganglia disease point to a role for corticobasal loop-systems, namely neocaudate-frontolateral and neocaudate-frontobasal circuits (Delong et al., 1983; Butters et al., 1985; Alexander et al., 1986; Kihlstrom, 1987; Heindel et al., 1988; Saint-Cyr et al., 1988). A recent PET study showed a corresponding increase of metabolic activity in the basal ganglia and the prefrontal associative cortex during the learning of two noncognitive procedural tasks (Perani et al., 1993). With regard to cognitive skills, Saint-Cyr and Taylor (1992) suggest that the neostriatum plays a role specifically in the early stage of learning. In Huntington’s Chorea, subnormal learning was found in a variant of the Tower of Hanoi task (Saint-Cyr et al., 1988). However, data on cognitive learning in patients with focal neostriatal or prefrontal lesions have not yet been published. Research on the cognitive mechanisms that underlie procedural learning has largely been limited to normal subjects. According to the influential ACT production model of skill acquisition (Adaptive Control of Thoughts; Anderson, 1982, 1983, 1987), cognitive procedural learning occurs in three stages through the generation, combination and improvement of condition-action pairs, referred to as productions. The first, the ‘‘declarative stage’’ of learning, involves the interpretation of task-relevant facts and knowledge. Nonspecific problem solving strategies (‘‘weak methods’’) are applied at this stage. Information about the problem and about task instructions needs to be represented in working memory and to be processed in multiple successive steps. The second, ‘‘knowledge compilation stage,’’ involves two processes: composition, i.e., unification of successive productions to larger and faster macroproductions, and proceduralization, i.e., translation of nonspecific productions into highly specialized productions that eliminate the need to hold explicit information in working memory. The third, ‘‘procedural stage,’’ is reached through continuous practice and is thought to lead to a refinement, tuning, and acceleration of established productions by means of strengthening, generalization, and discrimination processes, and by an increase of domain-specific working memory capacities. Ackerman (1988, 1990), Woltz (1988), and others (see Ackerman, 1987 for review) have examined the changing role of different cognitive abilities during cognitive skill acquisition in normal subjects. According to Ackerman

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(1990), at the declarative stage of skill learning, individual performance is determined by general ability measures such as intelligence, reasoning and working memory capacity, and by task-specific abilities (e.g., verbal, figural and numerical aptitude). During the knowledge compilation stage, perceptual speed abilities are considered the pricipal determinants of performance. During the procedural stage, performance is thought to improve according to a power law of practice, with the final level depending on psychomotor speed and accuracy. In amnesic patients, the learning of some perceptual (Cohen & Squire, 1980; Brooks & Baddeley, 1976) and motor skills (Milner, 1962; Corkin, 1968) has been found to proceed at a normal rate. Skills learned before the onset of the disease were shown to be retained (Squire et al., 1984; Della Sala & Spinnler, 1986). In contrast, the evidence for the learning of cognitive abilities in amnesia is inconsistent. In mixed-etiology groups of amnesic patients, normal progress was found for a computer-based task involving simple calculations and visual estimation (Squire & Frambach, 1990) and for a task involving the use of an artificial grammar (Knowlton et al., 1992). Ostergaard (1987) described an amnesic boy who was able to learn to play a computer game. On the other hand, two amnesic patients failed to learn to use an electronic memory aid (Wilson et al., 1989), and Beatty et al. (1987) found subnormal learning in the Tower of Hanoi task in a patient with posthypoxic amnesia. Subnormal learning was found in a maze task (Brooks & Baddeley, 1976; Nissen et al., 1989), in a concept formation task (OskarBerman, 1973), and in the Tower of Hanoi task (Butters et al., 1985) in Korsakoff patients. Charness et al. (1988) and Milberg et al. (1988) examined the learning of the mathematical skill of mentally squaring two-digit numbers in three amnesic patients. The declarative stage was bypassed by providing explicit instructions about the squaring algorithm. One Korsakoff patient and one patient with anterior communicating artery aneurysm improved with regard to overall time needed to solve the task, but showed little progress for single steps of the algorithm. Another aneurysm patient showed the reverse pattern. With reference to the ACT-model, this finding was interpreted to indicate a dissociation between subprocesses of the compilation phase. In summary, the data on cognitive skill learning in amnesic patients remain inconclusive. In regard to the cognitive mechanisms of procedural learning, it has been suggested that skill acquisition in amnesic patients is related to residual declarative memory capacity (Nissen et al., 1989; Squire & Frambach, 1990). This concept implies that cognitive skills involve a component of declarative memory and that procedural learning does not, or not entirely, occur in an implicit manner. An alternative hypothesis is that the variable performance of amnesic patients with regard to cognitive procedural learning is caused by concomitant deficits in general problem solving and in task-specific cognitive processing capacities. A corresponding suggestion has been made with refer-

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ence to Korsakoff patients’ subnormal learning of the Tower of Hanoi task (Charness et al., 1988). To date, the relationship of procedural learning, declarative memory and cognitive abilites in amnesic patients has not been studied experimentally. In order to test the aforementioned alternative hypotheses, we examined the learning of five cognitive tasks and one predominantly perceptual task in a group study involving 20 amnesic patients and 40 matched normal subjects. Three trials were carried out on consecutive days. Learning from the first to the third trial was analyzed with respect to group differences and within-group variations. Correlations were calculated between learning scores and residual declarative memory, as well as intellectual abilities assumed to be involved in the processing of the procedural tasks. We also studied the correlational relationship between the same intellectual abilites and absolute performances in the procedural tasks. The correlational patterns, the changes of these patterns that occurred following training of the tasks, and the differences in these pattern between control subjects and amnesic patients were analyzed with reference to the ACT production model of cognitive skill acquisition, and to Ackerman’s model of changing cognitive ability determinants. METHODS

Amnesic Patients Twenty amnesic patients were studied. Demographic data, memory scores and indices, intelligence indices (prorated), differences of intelligence and memory indices (IQ/MQ difference) and naming scores are listed in Table 1. The patients belonged to four diagnostic subgroups: • Five patients with ruptured aneurysm of the anterior communicating artery: These patients were operated on 2 to 15 months before the study. CT- and MRI-scans showed variable lesions of the basal forebrain, precallosal area and fornical columns caused by hemorrhage or ischemia. Patients 1 and 2 had a ventriculo-peritoneal shunt implanted for treatment of symptomatic hydrocephalus. The post-operative course for Patient 3 was complicated by meningitis. All patients exhibited mild to moderate frontal lobe signs (lack of initiative, distractibility, emotional indifference). Confabulation was observed in Patients 1, 2, and 5. • Four post-encephalitic patients: These patients were in the acute stage 2 to 29 months before the study. Epstein–Barr virus infection was diagnosed in Patient 6 and herpes simplex virus infection in Patient 7. In Patients 8 and 9, the infectious agent was not identified, but clinical findings strongly suggested a viral etiology. All patients were treated with Acyclovir. During the acute stage, imaging demonstrated variable involvement of the temporal, frontal and parietal lobes. At the time of the study, moderate dysnomia was still present in Patients 7 and 9. Patients 7, 8, and 9 exhibited mild to moderate psychomotor slowing and lack of initiative. Patient 9 could not perform tasks involving reading due to her poor reading ability. • Four patients with cerebral hypoxia: These patients suffered a hypoxic incident 2 to 13 months before the study. Causes were ventricular fibrillation (Patient 10), heroin intoxication (Patients 11 and 12), and an attempt at suicide by hanging (Patient 13). Imaging was unremarkable except for Patient 10, in whom diffuse hyperintensity of the frontal white matter was shown by an MR-scan 4 months postonset. This patient suffered general cognitive deterioration. Patient 11 showed mild psychomotor slowing and lack of initiative. Patients 12 and 13 appeared unimpaired upon clinical observation except for amnesia.

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TABLE 1 Demographic Data, Intelligence and Memory Scores of Amnesic Patients No.

Age, sex

Years of education

1 2 3 4 5 Mean

43, M 42, M 30, M 35, M 39, F 37.8

11 12 18 12 11 12.8

6 7 8 9 Mean

42, F 58, M 55, M 60, F 54.3

13 10 8 2 8.3

10 11 12 13 Mean

38, F 28, M 22, M 43, M 42.8

14 10 10 20 13.5

14 15 16 17 18 19 20 Mean

39, M 43, M 31, M 51, M 64, F 34, M 48, F 44.3

11 13 13 12 13 12 12 12.3

WAIS-R index

WMS-R score

Aneurysm patients 101 93 116 74 117 61 102 75 105 38 108.2 68.2 Encephalitis patients 138 130 84 65 89 52 70 38 95.3 71.3 Hypoxia patients 68 50 99 56 110 79 106 96 95.8 70.3 Korsakoff patients 82 28 96 83 109 89 77 53 108 79 100 86 84 69 93.7 69.6

WMS-R index

IQ/MQ difference

80 66 ,50 66 ,50 —

21 50 .67 36 .55 —

99 59 ,50 ,50 —

39 25 .39 .20 —

,50 ,50 59 81 —

.18 .49 51 25 —

,50 73 72 ,50 84 70 63 —

32 23 37 .27 24 30 21 —

Note. The WAIS-R index was prorated from eight subtests. The IQ/MQ-difference was calculated from WAIS-R and WMS-R indices.

• Seven patients with alcoholic Wernicke–Korsakoff syndrome: Onset of amnesia in these patients was 2 months to 7 years before the study. Psychomotor slowing, attention deficits and lack of initiative were observed in Patients 14, 17 and 18. Patient 15 exhibited a tendency toward confabulation. The other three patients appeared unimpaired upon clinical observation except for amnesia. Although individual differences in severity were evident upon testing and clinical observation, the amnesia was functionally incapacitating in all patients. At the time of the study four patients (1, 6, 7, 10) had returned to their families while the rest remained hospitalized. Five patients (3, 6, 7, 12, 19) recognized the task materials during the second and third days of testing. A General Memory index of 99 (Wechsler Memory Scale, Revised), present in Patient 6, was apparently inflated by superior short-term memory capacity (age-corrected Digit Span scaled score of 17), since this index is composed of tests which assess declarative memory without delay. This patient’s intelligence/memory index difference of 39 and her Delayed Memory index of 82 were clearly subnormal.

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Control Subjects Subjects were 40 unpaid volunteers, most of them dermatological patients or neurological in-patients being treated for peripheral nerve or spinal disk lesions. All subjects were free of CNS disease and were not taking any centrally active medication. Mean age (37.9 years in control subjects, 42.3 years in patients), distribution of sexes (55% males in control subjects, 70% males in patients), and years of education (mean 12.9 in control subjects, mean 11.9 in patients) did not vary significantly between the groups of patients and control subjects.

General Design To examine cognitive procedural learning, four new tasks and the Tower of Hanoi task were applied. The tasks were selected to involve a range of different cognitive capacities: problem solving (Tower of Hanoi), language (Sentence Arrangement), logical reasoning (Logical Reasoning, Concept Identification), and attentional processing (Mental Rotation). Except for the purely verbal Sentence Arrangement task, all tasks also involved a component of visuospatial processing. In addition, one predominantly perceptual task, Mirror Reading, was studied. Training of patients and control subjects was carried out in identical manner. The subjects were trained in three trials on consecutive days. Except for Tower of Hanoi, different parallel versions of the tasks were used during each trial. In a pilot study, the parallel versions were given to three groups of normal subjects in three different sequences; differences in mean baseline performance and learning were found to be minimal and nonsignificant. In all tasks, the measure of performance was time-to-completion, and the measure of learning was the progress made from the baseline trial to the third trial. In Tower of Hanoi, the number of moves required to complete the task was used as a second measure of performance. On each of the 3 days, the tasks were performed in fixed order. A complete session took 90 to 120 min. To ensure that the instructions were understood, example items were presented before each task. When necessary, instructions were repeated for every trial and task. Subjects were asked to work fast, but carefully. Information on solution strategies was not provided.

Procedural Tasks Logical Reasoning. Each trial of this task involved 12 problems, printed on cards. Each consisted of two written statements describing the relationship between three subjects or objects A, B, and C, followed by a question whose answer could be deduced from the information given. The relationships were concrete in nature, e.g., • A is heavier than B, but lighter than C. Who is the lightest? • A is much older than B. B is a little younger than C. Who is the youngest? • A has more money than B. C has less money than A. Who has the most money? Different relationships were used in each item. There were six different types of logical constructions, each applied twice per trial. Subjects were encouraged to convert the written statements into representational mental images of size. Paper and pencil were provided. When an incorrect solution was offered, the corresponding card was put at the bottom of the stack, until all problems had been solved correctly. The measure of performance for each trial was the time to complete all 12 problems. The three parallel versions of this task involved the same relationships and logical constructions, but their combinations varied. Sentence Arrangement. This task involved 20 problems per trial. Each contained five or six nonsensically ordered words that had to be arranged to form a meaningful and grammatically correct sentence in indirect speech. The sentence then had to be read aloud. Only one

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arrangement was possible. All sentences began with a personal pronoun, which was printed below as a prompt, e.g.: • anderes meine Redner glaubten etwas der (else meant speaker thought something the) (We...............................) Wir.............................. The measure of performance on each trial was the time required to complete the 20 problems. Different sets of sentences were used in the three parallel versions of this task. This task was omitted in Patients 7 and 11, who grew up in a different country and were not sufficiently familiar with German grammar, although they spoke the language fluently. Concept Identification. This task involved 15 problems per trial. Each consisted of a group of 12 symbols arranged in an area of about 100 sq cm. The symbols were characterized by six ‘‘concepts,’’ for each of which two expressions were possible: type (number or letter), shape (rounded or angular), orientation (regular or inverted), configuration (open or closed), symmetry (symmetrical or asymmetrical), and typeface (normal or bold). In each problem, all symbols shared one specific concept expression which the subjects had to identify, while the expression of the other five concepts was mixed. A list of the six possible solutions was always in view: ‘‘Possible common feature: letters, rounded shape, mirror-reverse, open shape, symmetrical shape, bold print.’’ Problems incorrectly answered were put at the bottom of the stack, until all problems had been answered correctly. Measure of performance was the time taken to solve all 15 problems correctly. The sequence of correct solutions was random. Different symbols were used in the three parallel versions of this task. Mental Rotation. Each trial involved five sheets with a different asymmetric symbol printed at the top of each (reference symbol). Below this, 16 alternative perspectives of this same symbol were arranged in a 4 3 4 fashion. These varying perspectives were achieved by rotating the reference symbol to different degrees. Eight of the 16 perspectives were also inverted. The instructions were printed at the bottom of each sheet: ‘‘Mark those symbols which can be derived from the reference symbol by rotation only.’’ For every error made, one-sixteenth of the time needed for this sheet was added. The measure of performance was overall time needed for all five sheets. While the same symbols were used in the three parallel versions of this task, the 4 3 4 arrangements of symbols were rotated and oriented in a different manner from trial to trial. Tower of Hanoi. This task serves as a standard task for the evaluation of frontal lobe function and of cognitive learning (e.g., Leon-Carrion et al., 1991; Goldberg et al., 1990; Schmand et al., 1992; Daum et al., 1993). It was performed according to the standard version (Simon, 1975) with four disks having to be moved from the left pole to the right pole without placing a larger disk above a smaller one or moving more than one disk at a time. The minimum number of moves is 15. This task was performed twice per trial, once at the beginning and once at the end of the session. Rule violations were corrected immediately. Two measures of performance were applied: the mean time, and the mean number of moves above 15 required to complete the task. One post-anoxic patient (10) with comparatively marked cognitive impairment could not solve the task. Mirror Reading. Each trial of this task involved eight lists of 10 six- to eight-letter-words. The words were printed mirror-reverse with a horizontal mirror axis, i.e., upside-down (but not backward). Subjects had to read the words aloud and correctly. Words that were not read correctly had to be attempted again at the end of the corresponding list. Measure of performance was the reading time taken for all eight lists (80 words). While different word lists were used in the three parallel versions of the task, they were uniform to the task in terms of first-letter distribution and frequency of ‘‘difficult’’ letters (b, d, h, p, q, n, u).

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Assessment of Procedural Learning In pilot studies, performance in the procedural tasks was found to vary considerably between subjects. However, individual baseline and third trial scores exhibited a close linear relationship. Therefore, absolute performance on the third trial, as well as absolute improvement from the baseline to the third trial were not suitable as indicators of learning, since these measures are biased by the individual level of baseline performance. The phenomenon of seemingly greater absolute gains in initially low-performing subjects was discussed by Ackerman (1987) in his review of individual differences in skill learning. He pointed out that treating the baseline performance as a covariate does not eliminate the problem. To remove the bias that is imposed by varying levels of baseline performance, we therefore employed a different measure of learning, namely, the quotient of final trial performance divided by baseline performance. This measure is applicable at early stages of skill acquisition, i.e., up to the point of practice when subjects begin to approximate a ‘‘ceiling’’ level of performance and the linear relationship between current performance and baseline performance is lost. To achieve complete independence of the applied measure of learning from individual variations in baseline performance, a minor modification was carried out. As shown by Figs. 1– 4, the regression lines that connect the control subjects’ data points cross the ordinate above the origin. This causes a bias toward numerically higher quotients (i.e., poorer learning) in subjects with numerically lower (i.e., better) baseline scores. To remove this bias, a constant was subtracted from third trial scores in each task, so that the control subjects’ regression lines crossed the origin. The same constants were subtracted from the patients’ third trial scores. The quotients of transformed third trial scores and original baseline scores are referred to as learning scores.

Assessment of Cognitive Abilities Cognitive abilities that were expected to play a role in the processing of the applied cognitive tasks were evaluated by standard neuropsychological tests. Tests of memory and language were given to amnesic patients only: To assess residual declarative memory in amnesic patients, the General Memory score from the revised Wechsler Memory Scale (WMS-R; Wechsler, 1987) was used. Verbal tasks were translated into German. Weighted raw-score sums, referred to as memory scores, were used in all statistical calculations. As a measure of language ability, an object-naming test was given to the amnesic patients except for those two who grew up in a different country (Patients 7 and 11). It involved 20 pictures from the Aachener Aphasie Test, 10 of which are single nouns and 10 compound nouns (Huber et al., 1983). Zero to 3 points were given per item; thus the maximum score was 60. The following tests were given to all subjects: As a measure of frontal lobe function, word fluency was evaluated by a six category fluency test (animals, fruit, furniture, girls’ names, birds, metals). Time-per-category was one minute. The sum of correct items for the six categories is referred to as fluency score. Word fluency tests serve as standard measures of frontal lobe function (Lezak, 1983a; Parker & Crawford, 1992), although scores may also be affected by dysphasia or psychomotor slowing. As a measure of visuo-spatial processing capacity, the scaled scores of two corresponding subtests from the revised German version of the Wechsler Adult Intelligence Scale (Tewes, 1991), i.e., Block Design and Object Assembly, were added to form a new score, referred to as visuo-spatial ability score. As a measure of general intellectual ability, the scaled scores of six further WAIS-R subtests, Digit Span, Arithmetic, Comprehension, Similarities, Picture Completion, and Digit Symbol, were added to form a general intelligence score. The Information- and Vocabulary

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subtests were omitted since they do not require cognitive processing; Picture Arrangement was omitted since this subtest may be disproportionately affected by frontal lobe dysfunction (Lezak, 1983b). The WAIS-R index (see Table 1) was prorated from the available eight subtests.

Statistical Analysis The distribution of all studied variables was examined with the Kolmogorov–Smirnov test. Significant deviations from normal occurred for naming scores in amnesic patients (p 5 .035) and for baseline scores in Concept Identification in control subjects (p 5 .045). The distributions of all other variables, i.e., cognitive abilities, absolute procedural task scores, learning scores, and age were not significantly different from normal within and across both subject groups. The effects of naming were analyzed using Spearman rank correlations. All other variables were analyzed by parametric statistical methods. Effects were considered significant if p , .05. Two-sided t-tests were applied to evaluate between-group differences in learning scores and absolute performance scores. Probability levels were corrected if variances differed significantly between groups. One-way analysis of variance (ANOVA) was applied to evaluate the role of cognitive abilities on between-group differences in learning. Kruskal–Wallis and Mann–Whitney rank analyses were applied to evaluate differences in learning between etiological subgroups of the amnesic patients. Pearson correlation coefficients and linear regression analyses were employed to examine the effects of cognitive abilities and age on absolute performance and learning in procedural tasks. Variables were considered independent determinants whenever the corresponding probability level was less than, or equal to 0.1 (statistical trend). With regard to the limited case number, regression analysis was not performed in the group of patients. Statistical calculations were performed with the SPSS-PC package, version 5.0.1.

RESULTS Cognitive Abilities

Declarative Memory This test was performed in amnesic patients only. Their mean WMS-R General Memory index was 63.6, their mean General Memory raw score was 69.7, and their mean Delayed Memory index was 57.3. Differences between General Memory indices and intelligence indices ranged from 20 to 67 points. Naming This test was also performed in amnesic patients only. Nine patients did not achieve the maximum socre of 60 for this test, indicating that they were mildly dysnomic (three aneurysm and three Korsakoff patients, one encephalitis patient, two hypoxia patients). The mean score was 57.6 (range 49–60).

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TABLE 2 Intercorrelations of Neuropsychological Test Scores and Age Intelligence Age Intelligence Visuo-spatial ability Fluency Memory

2.49*

Intelligence Age Intelligence Visuo-spatial ability

2.35*

Visuo-spatial ability

Fluency

Amnesic patients 2.32 2.33 .64** .49* .52*

Visuo-spatial ability

Memory

Naming

2.14 .69** .51*

2.60** .57** .44

.51*

.30 .18

Fluency

Control subjects 2.47** 2.05 .41* .39* .28

*p , .05, **p , .01.

Intelligence The mean scaled score sums of the applied six subtests was significantly higher in the control group (74.3 vs. 57.2, p , .001) The mean prorated WAIS-R intelligence index was 118.3 for control subjects and 98.1 for patients. Fluency Control subjects performed significantly better than patients in the sixcategory word fluency task (mean score: 115.3 vs. 63.2, p , .001). Visuo-spatial Ability Control subjects again performed significantly better than patients in this task (mean score: 24.1 vs. 17.7, p , .001). At all cognitive measures, mean rank differences between etiological subgroups within the group of patients were nonsignificant. Intercorrelations between cognitive abilities and age are listed in Table 2. Procedural Learning

In all tasks except Tower of Hanoi, absolute performances on the third trial and on the baseline trial were closely and significantly correlated (p ,

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FIGS. 1–4. Scatterplots of final trial scores versus baseline trial scores of three cognitive task examples and Mirror Reading. Continuous lines represent the regression lines of control subjects’ data. Data points above this line indicate lower-than-average learning. Note the presence of one outlier in Mirror Reading (Fig. 4), a woman with general intellectual impairment following cerebral hypoxia (Patient 10). FIG. 1. Logical Reasoning.

.01) in both subject groups. Correlation coefficients ranged from r 5 0.67 to 0.92 in the group of patients and from r 5 0.62 to 0.86 in the control group. The quotients of transformed third trial scores and untransformed baseline trial scores were applied as measures of learning as outlined above. Note that numerically lower learning scores indicate better learning. In the Tower of Hanoi task, a modified approach was applied (see below). Group differences of learning Figures 1–4 show the scatterplots of third trial scores versus baseline scores of four example tasks, which demonstrate substantial learning in both subject groups. However, it becomes evident that the group of amnesic patients made less progress in the cognitive tasks. The mean learning scores of amnesic patients and control subjects were compared with the use of two-sided t tests. With the exception of numberof-moves in the Tower of Hanoi task, significant between-group differences (p , .01) were present in all cognitive tasks, confirming superior learning in the group of control subjects. Conversely, learning scores in Mirror Reading were not significantly different between groups.

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FIG. 2. Concept Identification.

FIG. 3. Mental Rotation.

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FIG. 4. Mirror Reading.

The Role of Cognitive Abilities for Learning Procedural learning was analyzed taskwise in two steps. (1) Across and within subject groups, the effects of visuo-spatial ability, fluency, intelligence and age were examined by computation of correlation coefficients and by regression analysis of learning scores. Memory and naming, which were not assessed in control subjects, were included in the analysis of patients’ learning scores. Figures 5–8 show scatterplots of learning scores versus those variables that were identified as main determinants of learning across all subjects. The four example tasks correspond to those shown in Figs. 1–4. (2) The effects of visuo-spatial ability, fluency, and intelligence on the expression of between-group differences in learning were examined by analysis of variance (ANOVA). Logical Reasoning Across all subjects, learning scores were significantly correlated with visuo-spatial ability (r 5 20.48), intelligence (r 5 20.43), fluency (r 5 20.39) and age (r 5 0.34). Regression analysis identified visuo-spatial ability as the only determinant (p , .001). Within the control group, learning scores were significantly correlated with visuo-spatial ability (r 5 20.61) and age (r 5 0.44). Regression analysis confirmed both variables as independent determinants (visuo-spatial ability: p 5 .002, age: p 5 .098; excluding one outlier: p 5 .044 and .023, respectively). Within the group of patients, statistical effects of the examined variables were not observed.

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FIGS. 5–8. Scatterplots of learning scores versus those variables that were identified as main determinants of learning across all subjects. Continuous lines represent the regression lines of all subjects’ data. The tasks correspond to those shown in Figs. 1–4. FIG. 5. Logical Reasoning.

FIG. 6. Concept Identification.

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FIG. 7. Mental Rotation.

FIG. 8. Mirror Reading.

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In the ANOVA of learning scores, the main effect of subject group remained near-significant (p 5 .053) when visuo-spatial ability was entered as a covariate. The group effect was non-significant when intelligence (p 5 .115) or fluency (p 5 .142) were entered in addition. Concept Identification Across all subjects, learning scores were significantly correlated with visuo-spatial ability (r 5 20.41) and fluency (r 5 20.36). Regression analysis identified visuo-spatial ability as the only determinant (p 5 .002). Within the two subject groups, statistical effects of the examined variables did not reach significance. In the ANOVA of learning scores, the main effect of subject group remained significant whenever visuo-spatial ability (p 5 .001), or any other variable or combination of variables, were entered as covariates. Sentence Arrangement Across all subjects, learning scores were significantly correlated with intelligence (r 5 20.45), fluency (r 5 20.44) and visuo-spatial ability (r 5 20.28). Regression analysis identified intelligence as the only significant determinant (p 5 .050). Within the control group, statistical effects of the examined variables were not observed. Within the group of patients, learning scores were significantly correlated with naming (r 5 20.53, p 5 .029). In the ANOVA of learning scores, the main effect of subject group remained significant whenever intelligence (p 5 .033), or any other variable or combination of variables, were entered as covariates. Mental Rotation Across all subjects, learning scores were significantly correlated with fluency (r 5 20.43) and visuo-spatial ability (r 5 20.30). Regression analysis identified fluency as the only determinant (p 5 .001). Within the control group, there was a significant correlation with fluency only (r 5 20.42), but regression analysis identified age as an independent determinant (p 5 .035) in addition to fluency (p 5 .010). Within the group of patients, statistical effects of the examined variables were not observed. In the ANOVA of learning scores, the main effect of subject group was nonsignificant when fluency (but no other variable) was entered as a covariate (p 5 .255). Tower of Hanoi From the second day of training onward, control subjects’ scores (time and moves) were not significantly correlated with baseline scores, indicating the beginning of an approach toward ceiling performance. Thus learning

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could not be assessed in the same manner as in the other tasks. However, the two subscores that were obtained on the first and second execution of the task during the baseline trial were significantly correlated (p , .001). Learning scores were therefore computed from these two subscores, which reflect the initial progress made during the baseline trial. Time to complete the task. Across all subjects, learning scores were significantly correlated with fluency (r 5 20.39) and visuo-spatial ability (r 5 20.31). Regression analysis identified fluency as the only determinant (p 5 .003). Within the control group, statistical effects of the examined variables were not observed. Within the group of patients, there was again a significant correlation between learning scores and fluency (r 5 20.48, p 5 .039). The correlation with memory did not reach significance (r 5 20.41, p 5 .082). In the ANOVA of learning scores, the main effect of subject group was nonsignificant when fluency (p 5 .972) was entered as a covariate. Number of moves to complete the task. Across all subjects, effects of the examined variables did not reach significance. Within the control group, the correlation between learning scores and fluency approached significance (r 5 20.31, p 5 .068). Within the group of patients, a significant correlation between learning scores and fluency was present (r 5 20.51, p 5 .030). Mirror Reading Across all subjects, learning scores were significntly correlated with age only (r 5 0.31, p 5 .019). Regression analysis of learning scores confirmed age as the only determinant. Within the control group, an analogous result was obtained (r 5 0.48, p 5 .002 for age). Within the group of patients, statistical effects of the examined variables were not observed. Learning and the Etiology of Amnesia To analyze the possible effects of etiology on procedural learning, the learning scores of the four subgroups of amnesic patients were examined with the use of Kruskal–Wallis one-way analysis of variance (rank analysis for independent samples). Significant differences were not found for any task. Compared with the rest of the patients, aneurysm patients learned less at Tower of Hanoi, time-to-complete (mean rank 15.4 vs. 8.1, p 5 .010, Mann–Whitney U test). All other contrasts yielded no significant differences. Absolute Procedural Task Performance

The ranges of absolute performances in amnesic patients and control subjects overlapped broadly in all tasks (see also Figs. 1–4), but mean absolute scores differed significantly in favor of the control group. An exception was

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TABLE 3 Mean Absolute Scores and Mean Percentual Improvements in Procedural Tasks (Amnesic Patients/Control Subjects) Task Logical reasoning Sentence arrangement Concept identification Mental rotation Tower of Hanoi, time-to-complete Tower of Hanoi, moves . 15 Mirror reading

Third trial

Mean improvement

361/278 sec*

290/170 sec**

22%/37%

463/274 sec**

361/154 sec**

22%/42%

485/187 sec***

292/96 sec***

35%/45%

407/211 sec***

276/130 sec***

26%/38%

125/98 sec (n.s.)

79/40 sec***

36%/52%

5.7/6.0 (n.s.)

2.9/2.1 (n.s.)

40%/30%

714/315 sec***

351/155 sec***

47%/47%

Baseline trial

* p , .05, ** p , .01, *** p , .001. n.s., not significant.

the Tower of Hanoi task, where baseline scores were not significantly different. At later trials, a group difference in favor of control subjects increased progressively for time-to-completion, but remained minimal and nonsignificant for number-of-moves. Mean scores and mean percentual improvements are listed in Table 3. To analyze the role of cognitive abilities and age for absolute procedural task performances, Pearson correlation coefficients between the corresponding variables were calculated for both subject groups. Spearman rank correlations were calculated in the case of naming scores. Table 4 presents the correlation coefficients obtained on the first and on the third trial. In the control group, absolute procedural task scores were additionally examined by regression analysis. Intelligence, visuo-spatial ability and fluency were entered as independent variables. Those cognitive abilities that were correlated highest with absolute scores (see Table 4) were identified as the only determinants of the corresponding tasks. When age was included, an additional significant effect of this variable was found on the third trial in Logical Reasoning (p 5 .023) and on the baseline trial in Sentence Arrangement (p 5 .020). Age was identified as the only determinant on the third trial of Sentence Arrangement (p 5 .005) and on all trials of Concept Identification p , .01). DISCUSSION

Cognitive Abilities In the group of amnesic patients, mean intelligence, visuo-spatial ability and fluency scores were significantly lower compared to the control group.

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TABLE 4 Correlation coefficients of absolute procedural task performance with cognitive abilities and age on the first trial (baseline) and on the third trial. Significance levels as in Table 3. Task

Trial Intelligence

Logical Reasoning Concept Identification Sentence Arrangement Mental Rotation Tower of Hanoi, time Tower of Hanoi, moves Mirror Reading

1 3 1 3 1 3 1 3 1 3 1 3 1 3

2.54* 2.40 2.35 2.32 2.71** 2.69** 2.63** 2.58** 2.78*** 2.50 .11 2.27 2.47 2.52*

Logical Reasoning Concept Identification Sentence Arrangement Mental Rotation Tower of Hanoi, time Tower of Hanoi, moves Mirror Reading

1 3 1 3 1 3 1 3 1 3 1 3 1 3

2.33* 2.36* 2.21 2.18 2.43** 2.35* .00 2.14 2.08 2.08 .14 .00 2.34* 2.40*

Visuo-spatial ability Fluency Amnesic patients 2.05 2.45 .07 2.30 2.13 2.31 2.29 2.29 2.44 2.44 2.33 2.40 2.51* 2.40 2.57* 2.42 2.58** 2.46* 2.47* 2.35 .28 2.13 2.10 2.07 2.60** 2.44 2.60** 2.41 Control subjects 2.54** 2.23 2.70*** 2.23 2.37* 2.11 2.39* 2.04 2.23 2.13 2.29 2.09 2.38* 2.13 2.46** 2.36* 2.27 .10 2.46** 2.30 .07 .19 2.07 .00 2.47** 2.27 2.53** 2.36*

Age .30 .25 .05 .08 .43 .44 .54* .47* .49* .22 2.39 2.05 .14 .06

Memory Naming 2.19 2.14 2.50* 2.46* 2.60* 2.44 2.51* 2.46* 2.73*** 2.70** 2.12 2.26 2.52* 2.51*

2.49* 2.44 2.19 2.26 2.38 2.56* 2.58** 2.45 2.43 2.33 .43 .12 2.27 2.28

.33* .51** .41** .43** .42** .37* .05 .18 .22 .25 .15 .15 .12 .34*

Nine patients exhibited mild dysnomia. Significant differences between etiological subgroups were not found. The present cognitive deficits can be assumed to result from additional lesions outside the key structures of memory, which are present in many amnesic patients (e.g., Markowitsch & Pritzel, 1985). Cases of amnesia without accompanying cognitive deficits, e.g., following comparatively mild cerebral hypoxia (Volpe et al., 1983; Cummings et al., 1984; Zola-Morgan et al., 1986; Beatty et al., 1987), are in fact exceptional rather than common: widespread nerve cell losses may be present in posthypoxic (Adams et al., 1966) and post-encephalitic patients (Damasio & Van Hoesen, 1985); thalamic lesions are present in Wernicke–Korsakoff Syndrome patients (Victor

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et al., 1989); and lesions in prefrontal structures and connections are present following encephalitis (Eslinger et al., 1993), Wernicke encephalopathy (Joyce & Robbins, 1991; Butters et al., 1985; Baddeley & Wilson, 1988) and rupture of anterior communicating artery aneurysms (Donnet, 1993; Parkin et al., 1988). The Role of Declarative Memory and Cognitive Abilities for Procedural Learning Across all subjects, learning scores for cognitive tasks (but not for Mirror Reading) were significantly correlated with specific cognitive abilities, namely visuo-spatial ability in Logical Reasoning and Concept Identification, fluency in Mental Rotation and in Tower of Hanoi (time-to-complete), and intelligence in Sentence Arrangement. Within the control group, corresponding effects were observed in Tower of Hanoi, number-of-moves (fluency), Mental Rotation (fluency), and Logical Reasoning (visuo-spatial ability). Effects did not reach significance for those tasks where the analysis of patient data indicated a superimposition by effects of language or memory (these variables were not assessed in control subjects). Within the group of amnesic patients, learning scores were significantly correlated with fluency in Tower of Hanoi (both measures), and with naming in Sentence Arrangement. Indirect evidence for an effect of declarative memory was obtained in two tasks, where patients’ absolute performances were correlated highest with memory on all trials (Concept Identification) and on the third trial, respectively (Tower of Hanoi, time-to-completion; see Table 4). The cognitive abilities found to be related to procedural learning scores conform to the processing demands of the corresponding tasks: In Logical Reasoning, visuo-spatial processing was involved, since subjects were encouraged to convert the written statements into representational mental images of size relationships. In Concept Identification, the role of visuo-spatial processing is evident. Declarative memory can support the acquisition of this task, since explicit learning of the involved concepts reduces the time needed to consult the list of concepts. In Sentence Arrangement, the role of language ability, as assessed by naming, in learning is likewise evident. Across all subjects, intelligence was identified as a significant determinant of learning. This variable, which is composed of two non-verbal and four verbal WAIS-R-subtests, may be regarded as a related measure of verbal ability. In Tower of Hanoi, frontal lobe function, as assessed by fluency, is involved since the acquisition of this task requires rule-directed behavior, planning and problem solving, specifically at the initial stage of learning (Butters et al., 1985; Saint-Cyr et al., 1988; Goldberg et al., 1990; Schmand et al., 1992). It has been suggested that declarative memory plays an additional role for the learning of this task (Beatty et al., 1987). In the present

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study, the correlation of memory and patients’ learning scores did not reach significance. Indirect evidence for a role of memory was provided by high and significant correlations between memory and absolute performances (Table 4). This was the case for time-to-completion, but not for number-ofmoves, which may indicate that explicit learning of specific moves and subgoals accelerated the execution of the task, but did not support the improvement of strategy. Mental Rotation problems are employed as standard measures of visuo-spatial processing capacity. Accordingly, in the present Mental Rotation task absolute performance was correlated highest with visuospatial ability scores in control subjects. However, across and within both subject groups, fluency was identified as the only significant determinant of learning scores. It seems unlikely that executive frontal lobe functions, such as planning and problem solving, contributed in the learning of this task. However, the task demands other cognitive abilities that are attributed to the frontal lobes, e.g., controlled attentional processing and continuous switching between opposite mental sets (rotation/inversion). The Role of Age for Procedural Learning In the control group, the expected inverse effect of age on learning reached significance for three of the six tasks, i.e., Mirror Reading, Mental Rotation and Logical Reasoning. Conversely, an independent effect of age on absolute performance was observed in only one of these tasks on the final trial (Logical Reasoning). A relatively stronger effect of age on learning conforms to the general observation that the capacity for acquisition of new skills declines with increasing age, while aging affects the application of existing skills to a lesser degree. Group Differences in Procedural Learning In the perceptual Mirror Reading task, learning of amnesic patients and control subjects was not significantly different. This finding conforms to earlier results obtained with other versions of the same task (Cohen & Squire, 1980; Matrone et al., 1984; Beatty et al., 1987; Ewert et al., 1989). In the cognitive tasks, amnesic patients were significantly impaired relative to control subjects, although they made substantial progress. Their mean percentual improvement ranged from 22 to 40% (Table 3), and a proportion of patients showed entirely normal learning in each task (see Figs. 1–4). The relative success of patients with regard to their improvement on a range of new tasks, including a complex reasoning task (Logical Reasoning), confirms that cognitive procedural learning is, in principle, preserved in amnesia. In Tower of Hanoi, patients made normal progress with regard to the number of moves, while progress for time-to-completion was clearly subnormal. This suggests that normal progress for the number of moves was made at the cost of longer

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thinking times, and shows that considering the number of moves alone may be misleading. The relative deficit of amnesic patients in cognitive learning varied considerably according to task. To further investigate the factors that were related to group differences in learning, the learning scores were examined by ANOVA: In Mental Rotation and in Tower of Hanoi, time-to-complete, the main effect of subject group was nonsignificant when fluency, which was identified as a determinant of learning scores, was included as a covariate in the ANOVA, i.e. when the proportion of variance that was related to differences in fluency was considered. This result indicates that the group learning differences for these two tasks can be sufficiently explained by differences in fluency, i.e., frontal lobe function. In Logical Reasoning, the main effect of subject group remained near-significant when the corresponding variable, visuo-spatial ability, was included as a covariate. It was nonsignificant when either intelligence or fluency were included as additional covariates, suggesting that general and/or frontal lobe abilities played an additional role in the expression of group differences in learning of this task. In Sentence Arrangement and in Concept Identification, the main effect of group remained significant, regardless of which of the three cognitive abilities that were available across all subjects were entered as covariates in the ANOVA. This result indicates that other variables were pertinent to the expression of group differences in learning in these two tasks, e.g. language ability in Sentence Arrangement and declarative memory in Concept Identification. Compared to other patients, amnesic patients with anterior communicating artery aneurysm made significantly less progress in Tower of Hanoi, timeto-complete. This relative deficit was not accompanied by lower performance on fluency or declarative memory tests. Other differences between etiological subgroups were small and nonsignificant, suggesting that the specific pathology underlying the amnesic syndrome plays no important role in procedural learning. The Role of Cognitive Abilities in Absolute Procedural Task Performance Except for Tower of Hanoi, number-of-moves, control subjects attained significantly better absolute scores in all tasks (Table 3). The ratio of mean scores ranged from 1 : 1.3 to 1: 2.6 on the baseline, and from 1 : 1.7 to 1 : 3.0 on the third trial. The largest relative differences in favor of the control group occurred in Concept Identification, where patients’ performance was exclusively related to residual declarative memory capacity. The relationship of absolute procedural task performances and cognitive abilities is reflected by the correlation coefficients shown in Table 4. In amnesic patients, baseline scores were correlated highest with intelligence, except for Concept Identification and Mirror Reading. Conversely, in control sub-

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jects, baseline scores were correlated highest with visuo-spatial ability, except for the purely verbal task of Sentence Arrangement. Following practice, the correlations with intelligence decreased, whereas the correlations with visuo-spatial ability increased. In patients, the correlation between Sentence Arrangement and naming scores also increased following practice. Intelligence serves as a measure of general cognitive ability. Likewise, memory represents a general ability, in the sense of not being specific to certain types of skills. Conversely, visuo-spatial ability represents a more specific processing capacity, which was involved in most of the studied tasks. Language, as assessed by object naming, represents another task-specific ability. The present pattern of decreasing correlations with general abilities and increasing correlations with task-specific abilities conforms to the changing ability-performance correlations described by Ackerman (1986, 1988) and Woltz (1988) in their studies on cognitive skill learning in normal subjects. General ability measures have the highest power for predicting performance at the earliest stage of skill acquisition. According to the ACT-model, knowledge about the task at this stage has to be interpreted and translated into strategies and sequences of condition-action pairs. Performance depends on effortful, controlled processing. Parallel to the establishment of productions, the predictive power of general abilities declines, and task-specific abilities become more instrumental. In the present study, control subjects’ performance in procedural tasks was already correlated highest with visuo-spatial ability on the baseline trial, except for the purely verbal Sentence Arrangement task. This suggests that some learning took place as the subjects moved from problem to problem during the course of the first trial. Conversely, in amnesic patients, performance in the cognitive tasks was correlated highest with intelligence or memory throughout all trials. With reference to the cited model of practice-related changing ability-performance correlations, the prolonged dependence of amnesic patients’ performance on general abilities suggests that their transition from the initial, declarative stage to later stages of cognitive skill acquisition was delayed. Conclusions In the present study, a new methodology for the evaluation of the early stages of skill acquisition was applied. It removes the bias that is caused by differences in absolute performance level and allows an analysis of betweenand within-group variance in learning. Amnesic patients were found to make considerable progress in five cognitive tasks, but were significantly impaired relative to control subjects. Differences in learning were variably related to general and task-specific cognitive processing capacities. Indirect evidence suggestive of a role for residual declarative memory in skill acquisition was obtained in two tasks. Considering the design of the

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applied tasks, declarative memory appears to play a role only if the amount of explicit task knowledge instrumental to arriving at the solution exceeds the capacity of working memory. The absence of effects of memory in other tasks, including one involving complex reasoning, confirms that cognitive procedural learning can occur in a purely implicit mode and supports the hypothesis that concomitant deficits of cognitive processing capacities are crucial for deficits of cognitive procedural learning in amnesic patients. Comparable findings may be expected in patients with cognitive deficits due other types of brain lesions. The observed relation of absolute procedural task performance and various cognitive abilities conforms to existing models of cognitive ability determinants of learning. Together with the finding of inferior learning, the prolonged dependence on general abilities that was observed in amnesic patients suggests a slower and less efficient generation of strategies and ‘‘productions’’ in this group. In some of the procedural tasks, the cognitive ability determinants of learning and of absolute performance were found to be different: in Tower of Hanoi and in Mental Rotation, learning was related to fluency, while absolute performance was related to visuo-spatial ability, intelligence, or memory, and in Sentence Arrangement, patients’ learning was related to naming, while absolute performance was related to intelligence. Assuming that learning represents the generation and improvement of productions, and absolute performance represents the execution of existing productions, the present dissociation suggests that the development of productions can depend on cognitive and neuronal mechanisms that are different from those involved in their execution. REFERENCES Ackerman, P. L. 1987. Individual differences in skill learning: An integration of psychometric and information processing perspectives. Psychological Bulletin 102, 3–27. Ackerman, P. L. 1988. Determinants of individual differences during skill acquisition: Cognitive abilities and information processing. Journal of Experimental Psychology: General 117, 288–318. Ackerman, P. L. 1990. A correlational analysis of skill specificity: Learning, abilities, and individual differences. Journal of Experimental Psychology (Learning, Memory and Cognition) 16, 883–901. Adams, J. H., Brierley, J. B., Connor, R. C. R., & Treip, C. S. 1966. The effects of systemic hypotension upon the human brain. Clinical and neuropathological observations in 11 cases. Brain 89, 235–268. Alexander, G. E., Delong, M. R. & Strick, P. L. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Revue of Neuroscience 9, 357–382. Anderson, J. R. 1982. Acuisition of cognitive skill. Psychological Review 89, 369–406. Anderson, J. R. 1983. The architecture of cognition. Cambridge, MA: Harvard Univ. Press. Anderson, J. R. 1987. Skill acquisition: Compilation of weak-method problem solutions. Psychological Review 94, 192–210. Baddeley, A., & Wilson, B. 1988. Frontal amnesia and the dysexecutive syndrome. Brain and Cognition 7, 212–230.

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