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Research Reports |
PS Pohl, PT, PhD, is Associate Professor, Department of Physical Therapy, University of Florida, Gainesville, FL 32610 (USA) (ppohl{at}hp.ufl.edu).
JM McDowd, PhD, is Associate Professor, Department of Occupational Therapy Education, University of Kansas Medical Center, Kansas City, Kan
DL Filion, PhD, is Assistant Professor, Department of Psychology, University of Missouri-Kansas City, Kansas City, Mo
LG Richards, OTR, PhD, is Assistant Instructor, Department of Occupational Therapy Education, and Associate Scientist, Center on Aging, University of Kansas Medical Center
W Stiers, PhD, is Clinical Associate Professor, Department of Rehabilitation Medicine, University of Kansas Medical Center
Address all correspondence to Dr Pohl
Submitted June 19, 2000;
Accepted April 6, 2001
 | Abstract |
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Key Words: Cerebrovascular accident • Performance • Rehabilitation
| Introduction |
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"Implicit learning" is a broad term used to describe the acquisition of abstract knowledge without awareness of learning.5 For example, abstract grammatical rules may be learned implicitly during the acquisition of language.6 Procedural learning may be regarded as a subset of implicit learning in that it involves the learning of a perceptual-motor skill.5
One of the most common paradigms used to study implicit learning is serial response time tasks.7 Serial response time tasks have both perceptual and motor learning components and require the subject to respond to a stimulus, such as a light, with some motor response, such as touching it. Typically in research studies, the subject must attend to an array of 4 or more stimuli. The subject is instructed only to respond as quickly as possible to whichever stimulus lights up over a number of trials. What is not explained to the subject is that practice is organized in 2 ways: in 1 condition, the series of stimulus lights is presented in random order; in the other condition, a pattern for the presentation of stimulus lights is prescribed by the experimenter, and this pattern is repeated. Subjects are said to demonstrate learning of the pattern if their response time decreases during trials with the prescribed sequence and increases during subsequent trials with the random sequence.8 Subjects are questioned after practice is complete, and if they report not having noticed any sequence or pattern, their learning is said to be implicit. Other subjects may gain explicit knowledge of the task and report that they noticed something about the task (eg, they may have an impression that some lights follow other lights). Some subjects may have recognition or recall regarding the actual pattern of the sequence and can recognize the pattern when it is displayed or can reproduce it without cuing. Performance by these individuals reflects explicit learning.
Work by Boyd and Winstein9–12 was designed to examine the ability of people with stroke to learn by implicit and explicit means. In general, however, research that has examined motor learning in adults with stroke has focused on the instructions given to engage learners in explicit learning13–16; that is, subjects were told what they were to try to learn. Overall, the results of these studies suggest that individuals with unilateral stroke can learn motor skills when instructions are provided to give them the opportunity to function at an explicit level. It is not known whether adults with stroke can learn a motor skill implicitly.
There is now substantial evidence17–35 that implicit learning and explicit learning are controlled by different neural substrates. The functional neural network for implicit learning is thought to include the basal ganglia,17 cerebellum, and prefrontal cortex.18 The network for explicit learning is thought to include the temporal cortex, hippocampus, thalamus,19,20 and frontoparietal cortex.21 Learning differences in people with brain damage reflect, to a large extent, differences in neural substrates for implicit learning and explicit learning. For example, implicit learning, but not explicit learning, is preserved in some people with Alzheimer disease,22–25 amnesia,26 Huntington disease,27,28 and multiple sclerosis.29,30 In contrast, implicit learning is impaired in people with unilateral prefrontal cortex lesions,31 Parkinson disease,28,32,33 and cerebellar disease.32,34,35
Recently, it was shown that implicit learning is also dependent on the relationship between the side of the brain damage and the side of the effector, that is, the side of the limb performing the task. Implicit learning is preserved when adults with unilateral cerebellar lesions practice a task with the hand contralateral to the lesion, but this learning is impaired when practice is done with the hand ipsilateral to the lesion.36 In contrast, people with unilateral damage to the supplementary motor area37 or frontal area38 have impaired implicit learning involving the contralateral upper extremity (UE). Finally, people with callosal dysfunction can learn implicit tasks involving one hand, but cannot do so when both hands are required to respond to stimuli.38 Thus, it appears that the ability to learn implicitly depends on the integrity of the neuroanatomical substrates that subserve the performing UE.
Between 61% and 81% of strokes involve the anterior and middle cerebral arteries.39 The primary clinical manifestation of these strokes is hemiparesis. Even after 6 months or more, 45% of those who survive stroke are left with some degree of hemiparesis.40 Given that the primary deficits after stroke are on the side contralateral to the pathology, a unilateral stroke would leave the brain areas important for implicit learning intact if individuals performed a task with the UE ipsilateral to the lesion. Thus, it is reasonable to suggest that implicit learning would be preserved for people with unilateral stroke in the anterior circulation when performing with the UE ipsilateral to the lesion.
The primary purpose of our study was to examine the ability of adults with unilateral stroke to learn implicitly a motor skill using the UE ipsilateral to the side of brain damage compared with that of adults without stroke. If people with stroke can implicitly learn a serial response time task, performance would become faster during practice with a patterned, repeated sequence and would become slower with the introduction of a random sequence, and response time changes would be equivalent to those of people without stroke. If implicit learning is robust over time irrespective of unilateral brain damage, the speed of performance on a retention test 24 hours later should be similar between people with stroke and people without stroke.
A secondary purpose of our study was to investigate possible differences in the ability to learn implicitly relative to the severity of stroke. Given that the subjects performed the task with the UE ipsilateral to their brain damage, the severity of stroke should not affect implicit learning if implicit learning is dependent on an intact contralateral cortical substrate.
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Task and Equipment
The equipment used was a custom-made hand movement device (Fig. 1) consisting of 16 targets of 4 types of switches. Each type of switch was easily closed but required a different hand position (modeled after that of Harrington and Haaland45). We did not, however, specify a hand position for each type of switch. The first row (from the top) consisted of 2.54-cm-diameter knobs that were closed by turning them to the right or left. The second row consisted of switches (the size of standard light switches) that were closed by moving them to the right or left. The third row consisted of 2.54-cm-diameter buttons that were closed by pushing them in. The fourth (bottom) row consisted of switches (the size of standard light switches) that were closed by moving them up or down. A light was situated above each switch.
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Procedure
The rights of human subjects were protected. Participants signed a university-approved informed consent form that was part of a larger study evaluating attentional and learning capabilities of adults poststroke. The data from the motor learning task presented here are a subset of data collected. Participants with stroke used the UE ipsilateral to the side of brain damage; the UE that controls used was matched so that half used their left UE and half used their right UE. Participants practiced in 2 conditions: an 8-target patterned sequence and an 8-target random sequence. The participants were not informed that there were 2 conditions. The instructions were to close the switch corresponding to the light that became lit and to do so as quickly as possible. Practice was provided in an effort to ensure that the participant could close each switch properly.
Practice was conducted over 2 consecutive days and was organized into blocks. A block consisted of 10 repetitions of an 8-response sequence. A block was completed without interruption; that is, the closure of a target switch activated the subsequent target light to become illuminated. Subjects were given short rests of approximately 2 to 3 minutes as needed between blocks. On day 1, blocks 1 through 4 were the patterned sequence, blocks 5 and 6 were the random sequence and blocks 7 and 8 returned to the patterned sequence. The second day of practice was used as a measure of retention. Participants performed 2 blocks of the patterned sequence. Thus, participants performed a total of 100 8-response sequences; 80 of those were the patterned sequence.
A procedure commonly used to examine serial responses was used to assess explicit knowledge of the patterned sequence. In a recall test at the end of the retention measure on day 2, participants were asked whether they noticed anything about the task. Regardless of their response to this question, they were then informed that there was a patterned, repeated sequence embedded within their practice sessions. They were told to try to reconstruct that sequence by pointing to the switches (without the cuing of target lights) in the order that they thought represented the sequence. If they said they did not know, they were told to guess and to do the best they could.
Data Processing and Analysis
The sequence response time (SR) was recorded; this represented the time to complete a sequence of 8 stimuli and responses. Errors, such as moving the hand toward the incorrect switch or closing the wrong switch, were not counted individually but caused delays for the whole sequence and thus are reflected in the SR. The mean and standard error of the mean (SEM) of the SR were calculated for each 10 repetitions of an 8-response sequence to form blocks. The Statistical Package for the Social Sciences personal computer program (version 8.0)* was used for all analyses.
To examine differences between subjects with stroke and controls, 4 separate analyses of variance (ANOVAs) with a factor of group (stroke or control) and a repeated-measures factor of block were used to assess the following 4 items: learning of the patterned sequence, changes in performance with introduction of the random sequence, changes in performance with reintroduction of the patterned sequence, and retention. Effect size was calculated using an eta-square analysis (
2).46 Values of 2 of .01, .06, and .14 represent small, medium, and large effect sizes, respectively.46 A main effect of group would indicate a difference in SR between those with stroke and controls. If implicit learning is preserved in individuals with stroke, then there would be a main effect of block such that SR would become shorter with practice of the patterned sequence, SR would become longer when the random sequence is introduced, and SR would become shorter again when the patterned sequence is reintroduced. If implicit learning is retained in both groups, then there would be no main effect of group. For each analysis, group x block interactions would indicate differences in implicit learning between those with stroke and controls.
Explicit knowledge of the patterned sequence was assessed using a chi-square analysis. If individuals with stroke gain explicit knowledge as well as controls, then there would be no association between group and yes-no responses. The longest series of correct responses that subjects were able to generate was analyzed with a one-way ANOVA with group (stroke or control) as the factor. If individuals with stroke gain explicit knowledge as well as controls, then there would be no group effect.
To investigate whether adults with moderate stroke could learn implicitly, the data from the 27 subjects whose stroke severity had been defined as mild or moderate (ie, a subset of the large stroke group analysis) were analyzed in a 2-way ANOVA with a factor of group (mild or moderate) and a repeated-measures factor of block, with the same block comparisons as those aforementioned. In all of these analyses, the level of significance was P<.05, except for post hoc analyses, in which paired t tests were completed with a Bonferroni correction. The Greenhouse-Geisser method, a statistical method that makes the necessary adjustments for repeated measures,46 was used for all repeated-measures tests.
| Results |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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2=.163), reflecting decreased SR with practice. There was also a main effect of group (F=13.146, P<.002, 2=.140), reflecting the longer SR of those with stroke. The absence of a group x block interaction suggests that both groups improved performance at similar rates.
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2=.264), and there was a group x block interaction (F=3.358, P=.049, 2=.118). Post hoc analyses of the group x block interaction did not reveal differences between any pair of blocks for either group.
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2=.352). Individuals with stroke were slower than controls, as evidenced by the main effect of group (F=14.704, P=.000, 2=.154). There was no group x block interaction.
The SR of individuals with mild stroke increased 250±49 milliseconds, and that of individuals with moderate stroke increased 95±85 milliseconds. There was a main effect of group (F=5.662, P=.025, 2=.185), and there was a main effect of block (F=14.247, P<.001, 2=.363).
Enhancement of Performance With Reintroduction of the Patterned Sequence: Blocks 6 and 7
The reintroduction of the patterned sequence at block 7 resulted in faster SRs for those with stroke (55±21 milliseconds) and controls (29±12 milliseconds), representing improvements from block 6 of 4% and 3%, respectively. There was a main effect of block (F=9.801, P=.002, 2=.108), and there was a main effect of group (F=13.931, P=.000, 2=.147). There was no group x block interaction.
Sequence response times were 138±36 milliseconds faster at block 7 for those with mild stroke and 15±38 milliseconds faster for those with moderate stroke. There was a main effect of group (F=5.797, P<.025, 2=.188), there was a main effect of block (F=7.146, P<.014, 2=.222), and there was a group x block interaction (F=4.610, P=.042, 2=.156). Post hoc analyses revealed that the interaction was attributable to the faster SR in block 7 than in block 6 for those in the mild-stroke group only (t=3.885, P=.001).
Retention of the Patterned Sequence: Blocks 9 and 10
Controls and those with stroke decreased their SR over the 2 blocks of retention. There was a main effect of block (F=121.949, P=.000, 2=.601), and there was a main effect of group (F=11.781, P=.001, 2=.127).
The analyses of blocks 9 and 10 for those with mild and moderate strokes revealed a group x block interaction (F=6.522, P<.02, 2=.207). Post hoc analyses revealed that the SR for block 10 was faster than that for block 9 for both those with mild stroke (t=8.643, P<.001) and those with moderate stroke (t=8.034, P<.001).
Explicit Knowledge of the Patterned Sequence
With regard to whether participants noticed anything about the task, there was no difference between the participants with stroke and the control group, with most individuals stating that they noticed something (68% of those with stroke and 75% of controls). Similarly, there was no difference between those with stroke and the controls (2.2±0.3 and 2.8±0.4, respectively) for the largest number of correct single responses in a row recalled.
There was no difference in explicit knowledge of the patterned sequence between those with mild stroke and those with moderate stroke; two thirds of those with mild stroke noticed something about the task, and just over one half of those with moderate stroke did so. Subjects with moderate stroke did recall a larger number of correct responses in a row (3.7±0.7) than did those with mild stroke (1.7±0.4), as revealed by a one-way ANOVA (F=6.818, P<.02).
| Discussion |
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Although rehabilitation after stroke often has been based on the learning of motor skills, only within approximately the last 8 years has research provided some guidance regarding strategies for constructing practice for people with brain damage.47 Recently, the impact of instructions on rehabilitation has been discussed.48 Instructional strategies can provide the learner with explicit knowledge about the features of a task that are essential for performance of the task (ie, what a person needs to learn to achieve the goal associated with the task).3 Explicit learning is invoked when participants are searching for features, rules, or some structural property during practice and when they are able to say how they solved the problem.49 An alternative instructional strategy does not provide the learner with knowledge about the critical properties of the task, and the skill is learned implicitly.3 Implicit learning occurs when participants focus on specific items, such as searching for a target light, not rules, such as any relationship between successive target lights.49
In adults without neurological damage, there is evidence that explicit instructions can lead to poorer performance than implicit instructions.50,51 What instructional set is appropriate for people with stroke? Our results demonstrate that people with stroke, particularly those with mild stroke, can learn under implicit-learning conditions, suggesting that a strategy with implicit instructions may be important in rehabilitation. Studies are needed to compare explicit and implicit strategies to determine whether there is an optimal instructional set for adults with stroke.
The differences in performance between the participants with stroke and the older adults without impairments were attributable to the slower SR of those with stroke. This finding is congruent with the findings of researchers who have demonstrated that movements with the UE ipsilateral to the side of brain damage are slower than those in controls.15,16,52 In general, we suggest, as others have before,15,16,52 that the ipsilateral UE movement slowing may be attributable to disrupted output from the damaged hemisphere influencing the control of both UEs. An alternative, but not exclusive, explanation is that both hemispheres are necessary for normal execution of unimanual movements, particularly if the movements are complex.53–55
Implicit learning may be particularly appropriate for some people with stroke but not all. Contrary to our hypothesis, the performance of subjects with moderate stroke did not change as the practice condition changed even though the subjects performed with the UE ipsilateral to the lesion. It appears that the subjects were not able to learn the task implicitly and that the only learning that occurred was a nonspecific learning that allowed them to decrease SR and increase speed from the first block to the second block of retention. Given the small number of subjects with moderate stroke, we suggest that conclusions be drawn with caution. Damage in the neostriatum impairs implicit learning,32,56 and it may do so for both UEs. We did not have information about precise lesion locations. People with moderate stroke may have had greater involvement of the neostriatum than those with mild stroke.
Implicit learning is not a passive process,57 nor is it unconscious.58 The learner needs to be able to attend to the task that is practiced.7 Adults with stroke may have deficits in attentional processing.59 In our study, numerous trials were required. We chose a task that required different hand postures rather than the single hand posture that was required in the original serial response time task studies.7 We did this to make the task more interesting, although we admittedly have no measures of whether subjects were interested or attentive.
The presence of implicit learning suggests that there is no need to ask learners questions during practice about what they are experiencing,3 in sharp contrast to some of the techniques used in physical therapy. Whether there is a dichotomy in implicit learning and explicit learning is questionable.60 Indeed, some authors57,61 have argued that, with all learning, some parts of learning are explicit and some are implicit. An optimal strategy for motor learning within the context of rehabilitation may require some blend of explicit and implicit strategies that has yet to be defined, but at present this notion is speculative.
Implicit learning usually is thought to occur when changes in performance occur as the practice conditions change, such as a change from the patterned sequence to the random sequence in our study. The inclusion of a retention test is compatible with the motor learning literature in which learning is said to exist only with relatively permanent changes in behavior.4 The results of our retention test suggest that there was considerable retention of implicit learning for adults with stroke and controls. Group differences persisted in the retention test performance with the patterned sequence. However, both groups increased the speed of performance from the first block to the second block of retention. This result is congruent with research that has shown that implicit learning is robust49,62 and resistant to deterioration over time.62 However, we believe that caution must be exercised when generalizing the benefits of implicit learning to all measures of motor learning. Although retention tests have demonstrated the effectiveness of implicit learning, transfer tests have revealed that implicit learning can result in negative transfer.62 After implicit learning, performance deteriorated when subjects were asked to perform a task that was similar to but not exactly the same as the learned task.62 There was no transfer test in our study; however, no data suggested that transfer test performance would be any different for adults with stroke versus adults without stroke.
Explicit knowledge of a task learned under implicit-learning conditions does not appear to be different between individuals with stroke and older adults without impairments. A large percentage of subjects answered "yes" to the question about whether they noticed anything about the task. This open-ended question did not provide us with any information about what they noticed but was chosen to avoid leading the respondents as much as possible. However, the longest correct series recalled by members of either group was only approximately 2 out of the 8 responses. Thus, although subjects appeared, on the basis of questioning, to have some explicit knowledge, their recall performance was limited.
The relationship between the presence of explicit knowledge and the level of implicit learning in a task practiced under implicit-learning conditions has been debated in the literature.60,63 Explicit learning and implicit learning may occur in parallel, as suggested by the finding that those who train under explicit-learning conditions also gain implicit knowledge.60 Other researchers, however, have regarded the relationship between explicit learning and implicit learning as "antagonistic" (see, for example, Buchner et al63).
There are several limitations to our study. Using reports from medical charts, personal reports, and examinations, we limited our participants with stroke to those with unilateral lesions in what appeared to be the distribution of the anterior circulation system. We suggest that the results from our study should not be generalized to people with pathology in the brain stem or posterior circulation system or to those with bilateral brain damage. The diagnosis of stroke documented in medical charts for our subjects was based on a combination of clinical signs and symptoms and radiological information. Reports from brain imaging were not available for each subject. Without this information, it is not possible to verify the precise lesion size and location. We acknowledge that a branch of the middle cerebral artery serves subcortical areas, including the basal ganglia.64 In the absence of brain imaging reports, we cannot exclude the possibility that some of our participants with stroke had lesions that included the basal ganglia.
Another limitation of our study is that the participants with stroke were at least 6 months after onset of the stroke. We do not know whether implicit learning is intact during the early stages after stroke, when rehabilitation efforts are directed. This question remains to be answered. Our task was atypical and differed from the reaction time task used in serial response time paradigms. The nature of the task, that is, requiring different hand postures for responses, may have invoked more explicit-learning strategies than a task that requires only pushing buttons for each response. Finally, the individuals with stroke performed the perceptual-motor task with the UE ipsilateral to the lesion. Recently, it was shown that the primary sensorimotor cortex contralateral to the performing UE is active during implicit learning.21 In this light, we would predict that people with stroke could not learn implicitly with the contralateral, more affected UE. This notion remains to be empirically tested.
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| Footnotes |
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This study was approved by the Human Subjects Committee of the University of Kansas Medical Center.
* SPSS Inc, 444 N Michigan Ave, Chicago, IL 60611. 
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