In this work we found that the response to explicit information after stroke is uniformly disruptive regardless of task or lesion location. Based on current theories of timing control of discrete movements30,32 we had expected that explicit information might benefit implicit learning of discrete tasks, such as our SRT task. However, we found remarkable consistency across our tasks in that both stroke groups demonstrated an interference effect of explicit information. This point is particularly important for rehabilitation scientists who instruct clients during therapeutic tasks after stroke. Our data suggest that explicit information delivered before task practice is not as useful as discovering the solution to the motor task through practice alone.
Despite the interference effect that explicit information stimulated in individuals with stroke, it is important to note that all groups demonstrated implicit learning for both tasks (see Figure 4). A more precise interpretation of our data reveals that explicit information slowed or disrupted implicit learning; however, implicit learning was not arrested by the provision of explicit information. Of note is the improvement in performance seen for the BG-EI and SMC-EI groups when explicit information was not provided at the retention test (see Figure 3 difference between last block on day 3 and retention test).
We were surprised that no differences were noted when we compared implicit learning of continuous and discrete tasks. We expected that our discrete task might be more susceptible to the influence of explicit instructions. Previous work investigating timing control proposed that discrete tasks rely on a precise, event timing system where the brain possesses an explicit representation of the timed intervals necessary for task completion.30,32,43 Alternately, proponents of this event timing hypothesis43 suggest that continuous movements are indirectly timed and controlled by the use of emergent implicit strategies.30,43 Based on this previous work, it appeared plausible that discrete tasks would be more easily represented by explicit information and thus, performance and implicit learning might benefit from the acquisition of explicit knowledge. This assumption proved to be false. Not only did the BG-EI and SMC-EI groups not benefit from explicit instruction for the SRT task, but it actually induced an interference effect relative to that for the no-EI groups. Despite the HC-EI group's superior performance when provided with explicit information for both tasks, less change was evident during the discrete SRT than the continuous CT task for this group. This finding may represent a floor effect of our SRT reaction time measure. However, we believe that a more likely explanation is that the effect of explicit information during implicit motor sequence learning is consistent across task types and not differentially impacted by discrete versus continuous motor behaviors.
Our results that task type (as manipulated here) does not matter as explicit information seems to act uniformly on implicit motor learning confirm and extend our past work.1,2 To our knowledge this is the first study to consider the differential effects of continuous and discrete tasks during implicit motor learning. Though in the current study we did not find an effect of task, we recently reported that choice of implicit motor task does influence learning in some instances.44 In this work, we discovered that stroke severity was a major factor in determining how well participants' implicit motor performance improved during the practice of 2 discrete movement behaviors. In this case individuals with moderately severe strokes reacted uniformly to a functionally based implicit learning task and to the SRT. In contrast, healthy control participants and individuals with mild strokes showed more improvement on the functionally based task as compared to the SRT.44 The majority of participants in our current study had strokes that would be considered as moderately severe (using Fugl-Meyer scores, see Table 1). Because of their severity of stroke it is tempting to speculate that if we had tested a mildly affected group we might find differences between the CT and SRT tasks. We believe that this is unlikely, however, based on the pattern of performance of our healthy control group which was uniform across tasks and explicit information conditions (see Figure 4).
As mentioned our current results are consistent with previous work that has demonstrated an interference effect of explicit information after stroke.1,2 In addition, we once again found that explicit information benefits age-matched healthy control participants. These effects were noted for the BG-EI and SMC-EI groups even though they did not demonstrate full explicit knowledge for the sequence, particularly for the CT task (Table 4). This finding suggests that even minimal explicit awareness may alter implicit learning. Previous work has demonstrated that manipulating explicit knowledge (directed attention) during practice changes performance.45 We have extended this finding, as in this case, providing explicit instructions to individuals with stroke altered both acquisition performance and retention test ability.
Because we distinguished performance acquisition (practice) from implicit motor learning using a defined retention test we are able to make important distinctions when considering the impact of explicit information on implicit learning. Employing a retention test (administered after a one-day delay) allowed us to determine whether the effect of explicit information had a transient or more permanent effect on learning.46 We found that the effect of explicit information was relatively permanent, noting that the difference between the EI and No-EI groups was maintained despite the withdrawal of explicit information at the time of the retention test. This suggests a robust effect of explicit information on implicit motor learning which may have clinical ramifications.
Our data are a part of an emerging theme in the motor skill learning literature suggesting that implicit and explicit learning can either be separated and operate in isolation or impact and interact with one another.44 From these data and others1,2,24,47–50 it is becoming clear that the mixing of explicit and implicit is not necessarily beneficial for learning; in fact, it appears that after stroke in the basal ganglia or sensorimotor cortical regions it is at least temporarily harmful. Our demonstration of a detrimental effect of explicit instructions is not new,1,21,49,51 but only recently has this work begun to be extended into populations with neurologic damage.1,2 Poldrack et al has demonstrated that during learning the implicit and explicit systems may actually compete with one another for neural resources.24,52 These authors speculate that competition among memory systems may be due to incompatible demands during learning. The need for access to flexible knowledge maintained by the medial temporal lobe stands at odds with the necessity of fast, automatic responses supported by the striatum and motor cortex. Normally, this competition is managed by rapid, reciprocal patterns of activation in the medial temporal lobe, basal ganglia and motor cortex. Our data raise the possibility that damage to either a portion of the striatum or sensorimotor cortical regions disrupts this arbitration among memory systems and consequently impairs the usefulness of explicit information during implicit learning.
Regions within the SMC that are well understood to play a critical role in behavioral motor output include the primary motor cortex (M1), premotor cortex (PMC), and sensorimotor area (SMA). Ipsilateral M1 is active during the execution of complex, repetitive finger movements.53,54 Further, once explicit knowledge is gained for implicit motor behaviors neuroimaging shows that bilateral PMCs become active even during unimanual movements.55 This finding suggests that PMC has a strong role in regulating sequence production when learners have access to explicit information. The PMC has strong connections with prefrontal regions associated with explicit memories such as the dorsolateral prefrontal cortex (DLPFC) and is also reciprocally connected with the caudate nucleus of the basal ganglia.56,57 These neuroanatomic pathways appear to indicate that damage to the PMC and associated regions may disrupt the ability to integrate explicit information into implicit movements.
Similarly, the basal ganglia are richly connected with both motor cortical regions and the frontal cortex.57,58 At least 5 neuroanatomically distinct, reciprocal basal ganglia-thalamocortical circuits have been identified.59,60 It is assumed that these circuits allow the basal ganglia to have a widespread impact of the function of various cortical regions including the motor and prefrontal areas.58,60 The ‘motor’ circuit, which is comprised of the putamen, thalamus, SMA, and PMC, is thought to most directly affect movement.60,61 A separate ‘complex’ circuit has been identified that interconnects the caudate, thalamus, and DLPFC.58 The intricate complexity of the neuroanatomical interconnections between the motor and prefrontal cortex, and basal ganglia suggest that their combined action can facilitate high-level integrative functions. Our findings advance this conceptualization; we suggest that damage to the basal ganglia disrupted the interconnections with the prefrontal cortex that resulted in an inability to utilize explicit information during implicit motor learning.
Thus, we speculate that under normal circumstances, both the basal ganglia and the PMC are highly active to integrate explicit information into representations of movement (motor plans) as they are being learned. Our data suggest that disruption of either the basal ganglia or PMC results in an inability to benefit from explicit information during implicit motor learning.
Normally, motor performance of one hand invokes activity in the contralateral sensorimotor areas.55 Thus, in the past it has been incorrectly assumed that stroke does not directly affect the ipsilateral hemisphere. In this study and in numerous others1,2,22,26,44,62–65 there have been significant demonstrations of disrupted motor output using the arm ipsilateral to stroke. As both the SRT and CT tasks were entirely unimanual our finding suggests that bilateral hemispheric activity is necessary for executing and learning implicit motor sequence plans. Our data also show that stroke negatively affects the ability to use explicit information 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. We believe that these findings, along with others1,2,26,62,64,65 imply that therapeutic interventions must be directed to both the hemiparetic and the non-hemiparetic upper extremity after stroke.
Several conclusions may be drawn from our data. First, for healthy participants, explicit information appears to benefit implicit learning. Second, damage to the basal ganglia or sensorimotor cortex disrupts the capacity for explicit information to constructively influence the formation of an implicit motor plan over practice alone. Last, these findings were immune to the disparate demands of task domain (discrete or continuous). Our current data in combination with previous work lead us to believe that after stroke, some forms of explicit information are less helpful in the development of a motor plan than is discovering a motor solution through practice using the implicit system alone. Thus, the integrity of the basal ganglia and sensorimotor cortical areas may be crucial in determining the efficacy of explicit task information during implicit motor-sequence learning.
After stroke affecting the sensorimotor cortical areas or basal ganglia explicit information as provided here does not benefit implicit motor sequence learning regardless of the task domain. Because much therapeutic time is dedicated to motor skill acquisition after stroke this information is crucial for physical therapists that construct and implement conditions of practice and interventions designed to facilitate motor skill learning. It is likely that to optimize rehabilitation outcomes alternative methods of prescriptive information may be more useful to the learner than are explicit instructions. Other factors surrounding motor task performance for which there is growing evidence include focus of attention,60 visual feedback,66 extended practice,1,2,67 and success information.68–70 Clearly, exploring these alternate forms of explicit information and task conditions during implicit motor skill learning after stroke will be challenging for therapist and client alike, however, they may yield far more beneficial long-term results.
This research was funded by grants from the Foundation for Physical Therapy (PODS I and II awarded to LAB). Additional support was provided by the University of Southern California and the University of Kansas Medical Center.
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xi = participant's position in degrees at time 1, Ti = target position at time 1, n = the number of samples for the participant's trajectory array