Research Report
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Impact of Explicit Information on Implicit Motor-Sequence Learning Following Middle Cerebral Artery Stroke ўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўўў
Background and Purpose. Recovery of motor skills following stroke is supported, in part, by the implicit memory system. However, attempts to guide learning commonly use explicit instructions concerning “how to” perform a movement task. The purpose of this work was to systematically investigate the impact of explicit information (EI) on implicit motor-sequence learning using the ipsilesional arm in people with damage in the middle cerebral artery (MCA) distribution. Subjects and Methods. Ten people with unilateral stroke in the MCA distribution affecting the sensorimotor cortical areas and 10 people with no known pathology or impairment (control participants) were randomly divided into 2 groups. One group was provided with EI and one group was not (EI and No-EI groups, respectively) as the participants practiced an implicit motor-sequencing task over 3 days, with a retention test on day 4. Results. A 3-way interaction demonstrated that, across days of practice, EI had opposite effects on implicit motorsequence performance for the 2 groups. Post hoc tests confirmed that EI facilitated the performance of the control participants in the EI group but interfered with the performance of the participants with stroke in the EI group. This interference effect persisted, and was evident during the retention test in the participants with stroke in the EI group. Discussion and Conclusion. Explicit information was detrimental for implicit motor-sequence learning following MCA stroke. Rehabilitation outcomes may benefit from consideration of stroke location when determining the degree to which EI can augment implicit motor skill learning. [Boyd LA, Winstein CJ. Impact of explicit information on implicit motor-sequence learning following middle cerebral artery stroke. Phys Ther. 2003;83:976 –989.]
Key Words: Explicit information, Implicit motor learning, Physical therapy, Stroke.
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Lara A Boyd, Carolee J Winstein
Physical Therapy . Volume 83 . Number 11 . November 2003
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hysical therapists spend considerable therapeutic time explicitly delivering instructions to their patients and clients. In an effort to guide the learner to an optimal motor solution, these directions commonly are centered on “how to” complete a movement task. Despite the large amount of time and effort dedicated to instructing individuals during rehabilitation, few studies have considered the impact of explicit information on the learning of implicit motor skills in individuals with, or without, neurologic damage.1,2 In fact, no research has unequivocally established that verbal explicit instructions aid implicit motor skill learning in any population. This study sought to address this issue by investigating the impact of explicit information (EI) on implicit motor-sequence learning in people with stroke in the middle cerebral artery (MCA) distribution that affected the sensorimotor cortical (SMC) regions. Explicit Versus Implicit Memory and Learning Learning and memory are not singular processes, but are composed of many separate abilities. The broad categories of learning and memory can be subdivided into 2 main types— explicit and implicit.3 Explicit learning may be assessed directly by testing memory for
factual knowledge (eg, recognition and recall). In contrast, implicit learning is inferred by observing changes in skilled movement relative to some baseline performance. In this case, improved performance is assumed to reflect the acquisition of knowledge about the task, which is then manifested as, for example, faster or more accurate movements. Thus, the explicit and implicit learning and memory systems differ fundamentally. Explicit knowledge is represented as memory for facts, events, and episodes and may be formed very quickly (even following one exposure to explicit information). It is directly accessible to conscious recollection3 and is used to guide high-level cognition when decisions are based on complex rules and information. By contrast, the functions of the implicit system are highly distributed, supporting multiple behaviors, including skills and habits (eg, sequence learning), priming (eg, word completion), associative learning (eg, classic and operant conditioning), and nonassociative learning (eg, habituation).3 The focus of our study was implicit motor learning that subserves the acquisition of motor skills. The hallmark of implicit motor
LA Boyd, PT, PhD, is Assistant Professor, Department of Physical Therapy and Rehabilitation Sciences, University of Kansas Medical Center, 3056 Robinson, Mail Stop 2002, 3901 Rainbow Blvd, Kansas City, KS 66160-7601 (
[email protected]). Address all correspondence to Dr Boyd. CJ Winstein, PT, PhD, FAPTA, is Associate Professor, Department of Biokinesiology and Physical Therapy and Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, Calif. Both authors provided concept/idea/research design, writing, data analysis, and consultation (including review of manuscript before submission). Dr Boyd provided data collection, project management, fund procurement, and participants. Dr Winstein provided facilities/equipment and institutional liaisons. This research was approved by the institutional review boards of University of Southern California and Rancho Los Amigos National Rehabilitation Center. This study was supported by funding from the Neurology Section of the American Physical Therapy Association (Patricia Leahy Scholarship) and the Foundation for Physical Therapy (PODS Levels I and II) awarded to Dr Boyd. This article was received October 18, 2002, and was accepted June 25, 2003.
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learning is the capacity to acquire skill through physical practice without conscious recollection of what elements of performance improved. A classic example illustrating this process is learning to ride a bicycle. Improved performance is manifested by fewer falls, yet the ability to explicitly express “what” procedures are being used to avoid falling is almost impossible.4 The Interaction Between Implicit and Explicit Learning One of the most interesting features that separates the explicit and implicit learning and memory systems is their relative neuroanatomic isolation from one another. Strong evidence for this dissociation comes from the finding that individuals with medial temporal lobe damage demonstrate profound explicit learning deficits, but retain the ability to learn implicit motor skills.5–7 Fortunately, it is almost impossible to completely disrupt the implicit learning system to the same degree. Because the implicit learning system is highly distributed—supported by the cerebellum, basal ganglia, and SMC areas8 –13—the literature has shown that no single lesion or disease process completely abolishes the ability to implicitly learn and remember motor skills. Despite their neuroanatomic separation, it appears that explicit and implicit learning sometimes develop in parallel14 and can profoundly affect one another.1,15–17 This raises the possibility that one of these memory systems might be used to stimulate or inform the other. However, the mechanism for the interaction between explicit and implicit memory systems during learning is not yet understood. Recently, it was demonstrated that extended, focused implicit practice could be used to promote the explicit memory function in an individual with profound explicit memory loss.18 –20 Less studied is the impact of prior explicit information on motor-sequence learning in cases of an impaired implicit memory system. There are many examples demonstrating that the cognitive demand of explicit instructions can disrupt the formation of the implicit motor plan.15–17,21 This is true for rule learning16 and for implicit motor tasks.15 In these studies, it appears that EI interfered with participants’ implicit motor performance.22,23 These data suggest that explicit information was less helpful in the development of the motor plan for these tasks than was discovering a motor solution primarily through the implicit system. In contrast to the above referenced work, other data have been reported that demonstrate a benefit of EI for implicit motor skill learning.14 –24 These conflicting findings suggest that the impact of EI on implicit motor learning is dependent on the type, timing, and meaningfulness of the information provided. However, these factors have not been carefully considered.
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Implicit Motor Learning After Stroke-Related Brain Damage Another factor that may critically affect the impact of EI on implicit motor skill learning is lesion location following central nervous system damage. We have previously shown that EI aided implicit motor-sequence performance for individuals with stroke,1 but we did not consider the locus of brain damage.25 To date, only 2 studies have examined implicit motor skill learning in individuals with focal brain damage. These studies showed a benefit of EI following cerebellar stroke26 and an interference effect after basal ganglia stroke.21 However, no work has considered the impact of EI on implicit motor skill learning following focal brain damage resulting from stroke in the SMC areas. We expected that stroke in the SMC areas might negatively affect implicit motor skill learning. This is because the SMC regions are important for supporting movement initiation and fine motor coordination (primary motor cortex [M1]27,28), transitioning between movements (premotor cortex [PMC]29), and the selection of responses in a sequence when choices are based on internal or prelearned information (supplementary motor areas [SMA]30). Additionally, functional neuroimaging investigations commonly demonstrate both unilateral and bilateral activation in the M1, SMA, and PMC during implicit motor skill learning.8,11,13,30 –33 Stroke presents an excellent model for studying the neural control of learning because it permits investigators to examine the relationships between lesion location and functional deficits. This type of analysis allows the formation of hypotheses about regional brain contributions to behavior. One difficulty inherent in using a stroke model to study motor skill learning centers on the need to separate the effects of impairments in motor execution from motor learning. In this context, asking individuals with MCA stroke to use the more involved contralesional upper extremity for task practice is problematic; differences between people with and without stroke might be inflated by impaired motor execution and not reflect motor learning abilities at all. Further, individuals who did not have sufficient contralesional motor ability would be summarily excluded from all motor learning studies. We chose to circumvent these pitfalls by requiring individuals with MCA stroke to practice our implicit motor learning task using the ipsilesional upper extremity. It is well known that the motor control of both upper extremities is affected by unilateral stroke.34 –36 The bilateral participation of the SMC areas during motor sequencing tasks has been demonstrated in functional neuroimaging8 and by using transcranial magnetic stimulation that, when applied to the motor cortical areas, causes severe motor control deficits during motor-sequence practice.37,38 To expand
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ўўўўўўўўўўўўўўўўўўўўўўўўўўў Table 1. Participant Characteristics
Participants with stroke EIc No EI
Control participants EI No EI
Age (y)
Poststroke Duration (mo)
MMSEa
UpperExtremity Fugl-Meyer Motor Scoreb
Lesion Side
Sex
X
SD
X
SD
X
SD
X
SD
3 right, 2 left
2 male, 3 female
59.0
10.5
33.4
18.9
29.0
1.2
30.2
21.2
1 right, 4 left
4 male, 1 female
58.6
19.2
48.0
30.1
27.8
1.8
26.8
18.7
Age (y)
UpperExtremity Fugl-Meyer Motor Scoreb
Poststroke Duration (mo)
MMSEa
X
X
SD
Hand Used
Sex
X
SD
3 right, 2 left
1 male, 4 female
55.4
11.0
29.8
0.4
3 right, 2 left
2 male, 3 female
57.4
16.1
29.6
0.5
SD
X
SD
a
MMSE⫽Mini-Mental State Exam. Maximum upper-extremity Fugl-Meyer motor score⫽66. c EI⫽explicit information. b
on these data, we chose to determine if the disrupted ipsilesional motor control noted following MCA stroke would be mirrored by deficits in implicit motor learning. Therefore, the goal of this study was to examine the interaction between EI and implicit motor-sequence learning in individuals with unilateral damage in the SMC regions secondary to stroke in the MCA distribution. Based on our previous work,1 we hypothesized that EI would benefit sequence learning in people with no known neurologic damage as well as in those people with stroke in the MCA distribution as they practiced an implicit motor-sequencing task. Method Participants Ten people with first-time unilateral stroke in the MCA distribution affecting the SMC areas and 10 age-matched people with no known pathology or impairment (control participants) were recruited. All participants were randomly assigned to either a group that was provided with EI or a group that was not (EI and No-EI groups, respectively). Inclusion criteria for individuals with stroke were: (1) confirmation of unilateral damage in the MCA distribution affecting the SMC areas and (2) current clinical status being at least 6 months poststroke. To ensure homogeneity between the participants with stroke and the control participants, all participants were right-hand dominant (determined by participant self-report) and did not demonstrate any evidence of dementia (score of at least 26 on the Mini-Mental State Physical Therapy . Volume 83 . Number 11 . November 2003
Exam). Exclusion criteria for all participants included the following: (1) acute medical problems; (2) uncorrected vision loss; (3) previous history of psychiatric admission; and (4) history of multiple strokes, transient ischemic attacks, or extensive cortical white matter disease. Individuals with stroke were recruited from the outpatient clinical services at the University of Southern California Healthcare Consultation Center, the Rancho Los Amigos National Rehabilitation Center, and the South Bay Stroke Support Group. Control participants were recruited from the local community. To protect the individual rights of participants, each person signed an approved institutional informed consent form and a medical records release form prior to testing. To characterize stroke severity and ensure that no baseline differences existed between groups, the upper-extremity motor portion of the Fugl-Meyer physical assessment was calculated for each participant. There were no differences in age, Mini-Mental State Exam scores, or FuglMeyer motor scores between groups. Descriptions of the participants with stroke and the control participants are presented in Table 1. Lesion Location Prior to each participant’s inclusion in this study, review of an existing magnetic resonance imaging (MRI) or computed tomography (CT) scan confirmed lesion location. These medical records were obtained with the written consent of each participant. Existing MRI or CT scans were used to reconstruct each lesion on 3 representative axial brain slices.39 Each brain scan was reconstructed using custom-designed software. Representative Boyd and Winstein . 979
Figure 1. Lesion reconstructions for the participants with stroke in the explicit information (EI) and No-EI groups are displayed on 3 standardized axial slices from DeArmond and colleagues’ Structure of the Human Brain: A Photographic Atlas39 (slices 9, 10, and 11). The location of each axial slice is demonstrated by the sagittal slices at the bottom of the figure. None of the lesions extended below the lowest axial slice. Each brain scan was reconstructed using custom-designed software. (A) Participants in EI group (3 with right-side lesion, 2 with left-side lesion). (B) Participants in No-EI group (1 with right-side lesion, 4 with left-side lesion). SMC⫽sensorimotor cortical area.
overlay images demonstrating the extent of each individual’s brain lesion are illustrated in Figure 1. Instrumentation and Task All participants practiced the serial reaction time (SRT) task.6 Four different colored circles (yellow, red, blue, and green) could be displayed on the computer screen (43.2 cm [17 in], color) placed directly in front of the participant. A standard keyboard was placed on the table directly in front of the computer screen with the most centered letters (v, b, n, and m) capped with the colors yellow, red, blue, and green, respectively. Displaying 1 of the 4 colored circles on the screen generated stimuli for movement. Only 1 colored circle appeared at a time; the other circles were transparent. However, each colored circle always appeared in the 980 . Boyd and Winstein
same position and thus maintained its relative location on the screen and to the corresponding key. Following the appearance of 1 colored circle and prior to the display of the next colored circle, a large black asterisk, centered on the screen, served as a fixation point. Responses were made by pressing 1 of the 4 keys corresponding (in color and location) to the appropriately colored circle. A custom-designed computer software program (L Boyd, 2000, E-Prime software platform, version Beta 5.0)* controlled the appearance of the colored circles and recorded the participants’ responses. Time data (response time [RT]) were stored after every key press for future analysis.
* Psychology Software Tools Inc, 2050 Ardmore Blvd, Suite 200, Pittsburgh, PA 15221.
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Procedure Sequence practice. Participants were seated facing the computer screen with their hand resting on the keyboard. Participants with stroke used the hand ipsilateral to brain damage; the hand used by control participants was matched to that used by participants with stroke (Tab. 1). Four fingers of one hand were used to respond (all except the thumb). Following the cue to respond, participants pushed the key corresponding to the colored circle. Participants were instructed to “respond as quickly as possible.” The procedure for implicit repeating sequence practice was identical for both groups. All participants practiced the same fixed and repeating 10-element sequence (blue-yellow-red-blue-green-red-blue-red-green-yellow). This sequence was constructed to be ambiguous, such that there were minimal probability relationships among its elements. The beginning and end of each sequence were not marked, so that the transition between sequences was seamless. Each block of responses was composed of 10 repetitions of the sequence (100 responses). In each session, participants practiced the sequence a total of 50 times (5 blocks of practice). A short break of 1 to 2 minutes was provided at the end of each block of responses. An initial block of random responses were practiced (100 responses). Next, 4 blocks of repeating-sequence practice and a second block of random responses were performed. Finally, participants practiced 1 last block of the repeating sequence. In sum, participants practiced the repeating sequence for 5 blocks (50 times through the sequence, for a total of 500 responses) and made random responses for 2 blocks (200 responses). This practice pattern (1 random block, 4 sequence blocks, 1 random block, 1 sequence block) was repeated on 3 consecutive days. On day 4, retention tests were given to assess learning of the SRT task. Retention was measured by performance of 1 block of the repeating sequence. By random designation, half of the participants in each group were provided with explicit information regarding sequence patterns prior to practice, and half of the participants were kept unaware of the sequences being practiced. For those participants in the EI group, day 1 consisted of practice only. On day 2, participants in the EI group were informed that there was a repeating sequence in some of the practice trials. On day 3, participants in the EI group were explicitly instructed regarding the existence and composition of the repeating sequence. They also were provided with a schematic drawing of the repeating sequence that they were allowed to study, but not to physically practice. Days 1, 2, and 3 consisted of practice only for participants in the
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No-EI group; no explicit information regarding the sequence was provided. The delivery and content of explicit instructions for each group are detailed by day and group in Table 2. Explicit testing. Three levels of explicit knowledge were tested: subjective awareness of the existence and composition of the sequence, recognition memory, and recall memory. Subjective memories were tested by asking participants if they noticed anything about the task. Recognition memory tests determined if participants would be able to correctly identify the repeated sequence after watching it be played on the screen. Recall was tested to ascertain if participants knew the repeated sequence well enough to correctly predict what element of it would come next when viewing a fragment of the 10 elements (ie, 3 elements). Table 3 provides the instructions and details of explicit tests. Because of the differences in delivery of explicit information across groups, these tests were given at different time points. The EI group participated in 4 separate explicit test sessions (with only the first testing subjective awareness; Tab. 2). Explicit knowledge was tested for the No-EI group only after the retention test on day 4 (Tab. 2). Outcome measures. Response time (reaction time ⫹ movement time) was the time between stimulus onset to key press and was measured and stored for each trial. As is standard procedure in SRT task data analyses,1,6,8,14,40,41 we calculated the median RT for each 10-element sequence trial. Calculation of median RT values for each sequence trial reduces the sensitivity of this measure to very large or small values. Because RT data can be highly variable, the use of median RT as an outcome measure reflects a more conservative approach to data management.42 Response times then were summarized by calculating the mean median for each block of responses. This procedure was performed for both random and repeated sequences. Finally, to allow comparison across participants and to eliminate the effect of grossly different RTs, a change score was calculated for each block of practice (RT change score⫽mean median RT from the second block of random sequence practice on day 1 minus mean median RT from repeating sequence blocks 1–15). We chose to use the mean median RT from the second random block in all our change score calculations for 2 reasons: (1) at this time, the amount of practice and EI was equivalent between the EI and No-EI groups, and (2) we wanted to ensure that enough practice had occurred to greatly reduce (if not virtually eliminate) nonspecific learning effects. Early in practice, RT is often very long, but decreases rapidly as participants
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Subjective, recognition and recall
“Respond as fast as possible”
Explicit Test Condition
Explicit Test Questions
Subjective “Did you notice anything awareness about the task?”
If yes, “What was it?”
None
Watch 3 sequences: 1 True 2 False
“Is this a sequence that you recognize?”
Recall memory
Display 3 separate 4-element “What color comes sequence fragments (ie, next?” (forced yellow-red-blue-?) choice)
Data Analysis Acquisition performance was assessed using a 3-factor (group [participants with stroke, control participants] ⫻ information (EI, No-EI) ⫻ day [1, 2, 3]) analysis of variance (ANOVA), with repeated-measures correction for day and RT change score as the dependent measure. Subsequently, post hoc tests were performed to identify the locus of interactions. These tests separately examined information of the sequence (information ⫻ day ANOVA) and between-group differences (group ⫻ day ANOVA).
EI⫽explicit information.
None None None Explicit knowledge test
“Respond as fast as possible” “Respond as fast as possible” “Respond as fast as possible” Information condition No-EI
Recognition memory
become familiar with the task. These shorter RTs are often due to learning the relationship between stimulus and response and do not relate to sequence learning per se. To ensure that we did not inflate change scores by the inclusion of these nonspecific learning effects, we represented random response performance by using RT from the second random block (block 5 on day 1). Learning was assessed by calculating the difference between the median RT from the second block of random responses on day 1 and the mean median RT from the retention test. Explicit testing was evaluated by calculating a percentage-correct score for the subjective responses, recognition, and recall (eg, 80%, or 4 of 5 participants, noticed the repeating sequence).
a
None Prepractice test of recognition and recall Recognition and recall Subjective, recognition and recall Explicit knowledge test
Full explicit information: verbal instructions, study session, and pretest Partial explicit awareness: “Sequence exists” “Respond as fast as possible” Information condition EIa
Explicit Knowledge Test Conditions and Questions
If no, “There was a repeating sequence. Can you tell me what it was?”
Postpractice test of recognition and recall
“Respond as fast as possible”
Day 4 Retention Test Day 3 Postpractice Day 3 Prepractice Day 2 Day 1 Group
Explicit Information and Knowledge Testing Conditions by Group and Day
Table 2.
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Table 3.
Retention test data were used to reflect implicit motorsequence learning. These data were examined in 2 ways. First, the mean median RT from the retention test was compared with that from the random responses for each group and information condition (paired t tests). These results indicated whether implicit learning of the repeating sequence had occurred for each group. Second, the magnitude of RT change during the retention test was evaluated using a 2-factor (group ⫻ information) ANOVA. This analysis indicated whether normalized Physical Therapy . Volume 83 . Number 11 . November 2003
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Results
Figure 2. Change in response time (RT) for the repeated sequence across acquisition on the serial reaction time (SRT) task for control participants and participants with stroke in the explicit information (EI) and No-EI groups. Error bars are the standard error of the mean. The zero line represents random-sequence RT. Data below this line illustrate faster RT and reflect implicit motor-sequence learning. Solid lines reflect data for participants in the EI group; dashed lines reflect data for participants in the No-EI group. (A) Acquisition performance data across 3 days of practice for the control participants. (B) Acquisition performance data across 3 days of practice for the participants with stroke.
change scores were reliably different across group and information conditions. Post hoc 1-factor (information) ANOVAs were performed to determine the reliability of differences between groups that practiced with and without EI about the sequence.
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Acquisition Performance Regardless of the EI factor, all participants in this study were able to decrease their response times across acquisition, as indicated by their overall improved ability to respond to the practiced sequence relative to a random sequence (Figs. 2A and 2B; see days 1, 2, and 3). Visual inspection of the data, however, demonstrated that, contrary to our hypotheses, the participants with stroke did not benefit from the provision of explicit information. A full-factor ANOVA (with repeatedmeasures correction) confirmed this observation and revealed a 3-way group ⫻ information ⫻ day interaction (F⫽8.17; df⫽2,32; P⫽.00). Post hoc analyses revealed that EI differently affected the performance of the 2 groups. When the information factor was evaluated separately for each group (group ⫻ day ANOVA), performance was different between the participants with stroke and the control participants in the EI group (F⫽7.00; df⫽2,16; P⫽.05), whereas performance was not different between the participants with stroke and the control participants in the No-EI group (P⫽.21). When the 2 groups were considered separately (information ⫻ day ANOVA), both demonstrated an information ⫻ day interaction. However, the direction of this effect was opposite for the 2 groups. Providing the control participants with EI aided their performance (F⫽3.97; df⫽2,16; P⫽.04; Fig. 2A). In strong contrast to this result, EI impaired the ability of participants with stroke to reduce RTs (F⫽4.82; df⫽2,16; P⫽.02; Fig. 2B). These data are presented separately and in more detail in the following sections.
Control participants. Changes in RT for the repeated sequence across acquisition for the control participants are displayed in Figure 2A. Analysis of the change scores from days 1, 2, and 3 demonstrated improvements; both the EI and No-EI groups were faster in responding to the repeated sequence (main effect of day: F⫽15.16; df⫽2,16; P⫽.00). As mentioned earlier, the information ⫻ day interaction was due to the larger decreases in RT for the control
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participants in the EI group compared with the control participants in the No-EI group. By the end of practice on day 3, the control participants in the EI group had decreased RT by 196 milliseconds, whereas the control participants in the No-EI group had improved performance (decreased RT) by only 87 milliseconds. This difference indicates a clear benefit of EI during SRT task acquisition for individuals without neurologic damage. Because of our small sample size, we confirmed this finding by calculating an effect size.43 A large effect size (.72) verified that there was a meaningful difference between the control participants in the EI group and the control participants in the No-EI group at the end of day 3 of practice. Participants with stroke. The participants with stroke also were able to improve acquisition performance with practice (main effect of day: F⫽17.86; df⫽2,16; P⫽.00; Fig. 2B). The provision of EI, however, had a vastly different impact on the participants with stroke compared with the control participants. When given EI, the participants with stroke in the EI group demonstrated less change in their RTs relative to the participants with stroke in the No-EI group. This was confirmed statistically with an information ⫻ day interaction (see above). The detrimental effect of EI on individuals with stroke in the MCA distribution was most evident at the end of day 3 of practice, when the participants with stroke in the No-EI group demonstrated a 207-millisecond decrease in RT, whereas the participants with stroke in the EI group had decreased RT by only 128 milliseconds. This difference was meaningful, as demonstrated by a large effect size43 (.97), verifying the substantially better performance of the participants with stroke in the No-EI group than the participants with stroke in the EI group at the end of day 3 of practice. Retention Performance To demonstrate that there were no baseline performance differences between the EI and No-EI groups, random-sequence performance was compared for both the participants with stroke and the control participants. There was no difference between the participants with stroke and the control participants in the EI group in terms of random-response RT (Fig. 3A). Regardless of EI conditions, all of the individuals in this study demonstrated lower response times for the repeated sequence compared with the random sequence during the retention test (control participants in EI and No-EI groups, P⫽.01; participants with stroke in EI and No-EI groups, P⫽.05 and P⫽.03, respectively; Fig. 3). This finding demonstrates implicit motor-sequence learning of the repeated sequence, for both people with and without stroke affecting the SMC regions. Despite decreased RTs, neither the participants with stroke in the EI group
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nor those in the No-EI group were as fast in their responses as the control participants (Fig. 3A). A group ⫻ information ANOVA with the RT change score from the retention test as the dependent measure revealed an interaction (F⫽7.20; df⫽1,16; P⫽.02; Fig. 3B). Post hoc tests demonstrated that this interaction was the result of differences between the participants with stroke in the EI group and those in the No-EI group (F⫽5.20; df⫽1,9; P⫽.05). During the retention test, the participants with stroke in the No-EI group had decreased RTs compared with participants with stroke in the EI group (261 versus 138 milliseconds, respectively). Interestingly, there was not an information effect in the control participants during the retention test (P⫽.20). This finding indicates that, for individuals without neurologic damage, the beneficial effect of explicit information was temporary and principally affected acquisition performance. Explicit Knowledge Participants not provided with EI. The acquisition of explicit knowledge during implicit motor-sequence practice for both participants with stroke and control participants in the No-EI group varied greatly (Tab. 4). Most striking was the finding that, at the conclusion of 3 days of practice and the retention test, only 20% (1 of 5) of the participants with SMC-area stroke noticed the presence of some repetition in their responses. In contrast, 80% (4/5) of the control participants in the No-EI group reported being aware of a repeating sequence for some of the trials. Despite this disparity, the control participants and the participants with stroke in the No-EI group were similarly poor in their ability to recognize (66% and 53%, respectively) and recall (40% and 33%, respectively) the practiced sequence. The poor recall performance of both the control participants and the participants with stroke (below 50%) indicates that they were guessing and unable to correctly recall the repeated sequence. Participants provided with EI. Similar data were found at the conclusion of day 1 of practice when explicit knowledge was first tested in both participants with stroke and control participants provided with EI. Eighty percent of the control participants in the EI group stated that they noticed some degree of repetition in their responses for the SRT task (Tab. 5). Despite this, recognition and recall were below chance (40% each). By the end of day 2 of practice, recognition for the control participants in the EI group had improved to 73%; however, recall remained below chance (40%). After the study period, the control participants demonstrated a high degree of explicit knowledge of the SRT task prior to (recognition
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86%, recall 73%) and at the end of (recognition 100%, recall 86%) practice on day 3. The participants with stroke in the EI group demonstrated poor knowledge of the sequence at the end of day 1 of practice (20%; Tab. 5). Recognition was at a chance level (46%), and recall was below chance (27%). Over day 2 of practice, when the participants with stroke explicitly knew that a sequence existed, they showed improved recognition (53%) and recall (47%). The pre-implicit practice, explicit study period at the beginning of day 3, substantially improved sequence recognition (80%), but not recall (47%). Following sequence practice on day 3, recognition was well above chance (73%), and recall was just at chance level (53%). Discussion There is little agreement in the literature concerning the impact of EI on implicit motor-sequence learning. Further, few studies have addressed the question of the effect of EI on implicit motor-sequence learning with regard to the neural substrates that may mediate this information transfer. This was one question addressed by this study: How might EI affect implicit motor-sequence learning following focal stroke in the neural regions that likely subserve learning and may mediate information transfer between the explicit and implicit memory systems?
Figure 3. Retention test data for control participants (HC) and participants with stroke in the middle cerebral artery distribution that affected the sensorimotor cortical regions (SMC) in the explicit information (EI) and No-EI groups. Error bars are the standard error of the mean. (A) Absolute mean median response time (RT) for repeated versus random sequence during the retention test on the serial reaction time (SRT) task. The difference between repeated and random sequence reflects learning. There were no baseline differences between the control participants and participants with stroke in the EI and No-EI groups. Regardless of EI condition, the performance of the participants with stroke was slower than that of the control participants. (B) Change in RT for the repeated or “learned” sequence as compared with random-sequence performance during the retention test. Explicit information interfered with learning in the participants with stroke in the EI group.
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We hypothesized that EI would benefit both groups’ implicit motorsequence learning. We learned, however, that this was not true for individuals with stroke affecting the SMC areas. Participants with stroke in the EI group were unable to make use of EI during acquisition performance. Indeed, they demonstrated poorer learning of the SRT task than did participants with stroke in the No-EI group. This pattern suggests an interference effect of EI on implicit motorsequence learning, and that explicit
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Table 4. Explicit Knowledge of Participants Not Provided With Explicit Informationa
a
N
Subjective % Noticed
Recognition % Correct
Recall % Correct
Control participants
5
80 (4/5)
66.0
40.0
Participants with stroke
5
20 (1/5)
53.0
33.0
Scores below 50% indicate responding at or below chance (ie, guessing).
information might have blocked formation of the implicit motor plan. Regions within the SMC have long been considered critical for most motor output (including the M1, PMC, and SMA). It has been demonstrated that ipsilateral M1 is active during the execution of complex, repetitive finger movements.37,38,44 Further, neuroimaging data have shown that once EI is gained for implicit tasks, bilateral PMCs are active even for unimanual tasks.30,45 This finding suggests that the PMC has a strong role in regulating sequence production when learners have access to EI. Interestingly, the PMC has strong connections with the prefrontal regions associated with explicit memories (ie, the dorsolateral prefrontal cortex) and is richly and reciprocally interconnected with the caudate nucleus of the basal ganglia.46 – 48 It is quite likely that damage to, and in regions associated with, the PMC results in disrupted integration of EI into planned sequences of movement. Similarly, we also have reported that following basal ganglia damage, EI has a large interference effect on implicit motor-sequence learning.21 Perhaps under normal circumstances, both the basal ganglia and the PMC are highly active in the integration of EI into the representations of movement (eg, motor plans) that are being learned. It may be that disruption of either of these regions leads to diminished ability to take advantage of EI during implicit motorsequence practice. Explicit information affected acquisition performance differently for both groups of participants. Explicit information clearly benefited the control participants in the EI group, as demonstrated by the larger decreases in RT for these participants compared with the control participants in the No-EI group and participants with stroke in both the EI and No-EI groups. The beneficial impact of EI on the acquisition performance of individuals without neurologic damage corroborates previous findings by Curran and Keele.24 However, Curran and Keele’s findings contradict work by Reber and Squire,7 who did not find a benefit of prior EI for a group who memorized the sequence before practice.
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There are 2 logical explanations for this disparity. First, no pretest was administered in the study by Reber and Squire,7 and it cannot be assumed that the participants had explicitly learned the sequence. We controlled for this factor by using a pretest to demonstrate that both the participants with stroke and the control participants in the EI group showed a high degree of recognition memory for the repeated sequence prior to practice at the beginning of day 3 of practice (Tabs. 2 and 5). A second difference centered on the timing of the provision of EI. In our study, participants in the EI group had an initial 5 blocks of sequence practice without any EI; another 5 blocks were practiced with partial EI (of the existence of a sequence). Finally, at the beginning of day 3 of practice, full EI was provided. Thus, all participants in the EI group had considerable amounts of implicit SRT task practice before they were encouraged to incorporate EI into their performance. It has been hypothesized that explicit and implicit memories develop in parallel, but that awareness of EI does not occur until a certain degree of motor success has been achieved.14,49 If this is true, then perhaps it is not just awareness of EI that occurs following some motor success; more importantly, EI may only be incorporated into, and benefit, the motor plan after some degree of implicit task ability has been gained. It has been demonstrated that when sequences are practiced unilaterally under purely implicit conditions, SMC regions are more active contralaterally.30,50 Therefore, it has been assumed that the ipsilateral SMC function is not directly impaired by stroke. In our study, the participants with stroke in both the EI and No-EI groups initially showed very long RTs, which reflects disrupted motor output. This detail is interesting, as the individuals with stroke were practicing using the arm ipsilateral to brain damage, and thus their undamaged cortical hemisphere and less-involved upper extremity. As the SRT task was unimanual, this finding suggests that bilateral hemispheric activity is used for executing and learning motor sequence plans. Indeed, other work has shown that ipsilesional deficits after stroke affect rehabilitation outcomes.51–53 Our data demonstrate that, in addition to impairing motor control,34,54 MCA stroke also negatively affects the ability to use EI during implicit motor task practice, even when using the ipsilesional upper extremity. As use of the ipsilesional arm invoked the undamaged hemisphere, the performance deficits we recorded strongly suggest that bilateral hemispheric function is necessary during implicit motor-sequence learning. Our findings, along with the findings of other researchers,35,54 imply that, in the clinical arena, therapeutic interventions also must be directed to the less-involved upper extremity following MCA stroke.
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ўўўўўўўўўўўўўўўўўўўўўўўўўўў Table 5.
Explicit Knowledge of the Participants Provided With Explicit Informationa
N
Subjective % Noticed
Day 1 Control participants Participants with stroke
5 5
80 (4/5) 20 (1/5)
Day 2 Control participants Participants with stroke Day 3 pretest Control participants Participants with stroke
Recognition % Correct
Recall % Correct
40.0 46.6
40.0 26.6
5 5
73.0 53.3
40.0 46.6
5 5
86.6 80.0
73.0 46.6
ally, because of the unique nature of the implicit learning and memory systems, it may be problematic to extend these findings to all of motor learning. Last, due to our small sample size, it may be premature to alter clinical practice solely on the basis of these data. Therefore, it may be prudent to wait for future data to confirm or refute our findings before making dramatic changes in rehabilitation practice.
Conclusion Consideration of the locus of brain Day 3 posttest damage in conjunction with the speControl participants 5 100.0 86.0 cific behavioral function associated Participants with stroke 5 73.3 53.3 with the region of stroke during formaa Scores below 50% indicate responding at or below chance (ie, guessing). Explicit knowledge tests of tion of the rehabilitation plan may be participants provided with explicit information were performed at the end of each day of practice. In one means of optimizing recovery of addition, a pretest of explicit knowledge was administered at the beginning of day 3. Subjective awareness of the sequence was assessed only at the end of day 1. function poststroke. Bilateral SMC areas are likely important for accurate formation of the motor plan for moveThe findings of this study might inform clinical practice ment. For the participants in this study, it appears that, in several ways. We documented that, regardless of following SMC stroke, EI did not benefit SRT task information condition at the time of the retention test, learning and in fact it degraded both performance and the performance of the participants with stroke was learning. We believe that other alternative methods of never as fast as that of the control participants. Thus, this prescriptive instructions (other than verbal explicit study adds to the growing body of literature demonstratinformation) might have been more beneficial for ing that the ipsilesional upper extremity is not comimplicit learning of motor skills in this sample. This idea pletely spared from the effects of MCA stroke.34 –36,51–55 is not new57; however, its implementation into the clinDespite this finding, it is critical to remember that all of ical environment would require substantial reconceptuthe individuals with MCA stroke in our study demonalization. For example, it is possible that explicit instrucstrated the capacity for implicit motor-sequence learntions should be used to focus the learner’s attention ing. This is an important fact, and supports other recent rather than provide information about the task.58 Mak41 work by Pohl et al. It appears that, with sufficient ing such a paradigm shift in the rehabilitation setting practice, improved acquisition performance can persist may prove initially difficult for therapist and client alike, (retention performance), and the motor task can reliyet it may yield far more beneficial long-term results. ably be considered learned. References
The predominant pattern of stroke is in the distribution of the MCA56 and affects the SMC areas and the basal ganglia. Currently in clinical practice, it is common for little attention to be paid to the locus of brain damage (other than identifying which side of the brain is affected). It is clear that individuals in this study who had stroke affecting the SMC regions did not benefit from EI during SRT learning; more accurately, EI interfered with learning in this group. It is very difficult to extend laboratory data directly into clinical practice; however, we believe that consideration of lesion location, and increased awareness of the type and timing of EI about the task, might benefit implicit motor learning following stroke. However, several factors limit the generalizability of our findings. We are not able to form any conclusions regarding the impact of lesion in the right versus left hemisphere on implicit motor skill learning. Addition-
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