Frames of reference during implicit and explicit learning

There is a significant overlap between the processes and neural substrates of spatial cognition and those subserving memory and learning. However, for procedural learning, which often is spatial in nature, we do not know how different forms of spatial knowledge, such as egocentric and allocentric frames of reference, are utilized nor whether these frames are differentially engaged during implicit and explicit processes. To address this issue, we trained human subjects on a movement sequence presented on a bi-dimensional (2D) geometric frame. We then systematically manipulated the geometric frame (allocentric) or the sequence of movements (egocentric) or both, and retested the subjects on their ability to transfer the sequence knowledge they had acquired in training and also determined whether the subjects had learned the sequence implicitly or explicitly. None of the subjects (implicit or explicit) showed evidence of transfer when both frames of reference were changed which suggests that spatial information is essential. Both implicit and explicit subjects transferred when the egocentric frame was maintained indicating that this representation is common to both processes. Finally, explicit subjects were also able to benefit from the allocentric frame in transfer, which suggests that explicit procedural knowledge may have two tiers comprising egocentric and allocentric representations.     

Prefrontal and striatal activation in elderly subjects during concurrent implicit and explicit sequence learning

Decreased function in the prefrontal cortex (PFC) is regarded as a primary mechanism of cognitive aging. However, despite a strong association between the prefrontal cortex and the neostriatum, the role of the neostriatum in cognitive aging is less certain. In the current study, event-related functional MRI was used to distinguish the cognitive contributions of neostriatal and prefrontal function in elderly versus young subjects. Twenty healthy subjects, 9 elderly (mean age 67.6 years), and 11 young (mean age 22 years) performed a concurrent implicit and explicit sequence learning task while undergoing functional MR imaging. Both groups showed learning in both the implicit and explicit task conditions. Relative to the young subjects, the elderly subjects showed decreased activation in the left PFC during both implicit and explicit learning, decreased activation in the right putamen during implicit learning, and increased activation in the right PFC during explicit learning. Our results support the theory that changes in a network of brain regions, including the dorsolateral prefrontal cortex and the striatum, are related to cognitive aging. Moreover, these changes are observed during an implicit task, and thus do not seem to be mediated by awareness.     

Effects of learning with explicit elaboration on implicit transfer of visuomotor sequence learning

Intervals between stimuli and/or responses have significant influences on sequential learning. In the present study, we investigated whether transfer would occur even when the intervals and the visual configurations in a sequence were drastically changed so that participants did not notice that the required sequences of responses were identical. In the experiment, two (or three) sequential button presses comprised a “set,” and nine (or six) consecutive sets comprised a “hyperset.” In the first session, participants learned either a 2 × 9 or 3 × 6 hyperset by trial and error until they completed it 20 times without error. In the second block, the 2 × 9 (3 × 6) hyperset was changed into the 3 × 6 (2 × 9) hyperset, resulting in different visual configurations and intervals between stimuli and responses. Participants were assigned into two groups: the Identical and Random groups. In the Identical group, the sequence (i.e., the buttons to be pressed) in the second block was identical to that in the first block. In the Random group, a new hyperset was learned. Even in the Identical group, no participants noticed that the sequences were identical. Nevertheless, a significant transfer of performance occurred. However, in the subsequent experiment that did not require explicit trial-and-error learning in the first session, implicit transfer in the second session did not occur. These results indicate that learning with explicit elaboration strengthens the implicit representation of the sequence order as a whole; this might occur independently of the intervals between elements and enable implicit transfer.     

Simultaneous sensorimotor adaptation and sequence learning

Sensorimotor adaptation and sequence learning have often been treated as distinct forms of motor learning. But frequently the motor system must acquire both types of experience simultaneously. Here, we investigated the interaction of these two forms of motor learning by having subjects adapt to predictable forces imposed by a robotic manipulandum while simultaneously reaching to an implicit sequence of targets. We show that adaptation to novel dynamics and learning of a sequence of movements can occur simultaneously and without significant interference or facilitation. When both conditions were presented simultaneously to subjects, their trajectory error and reaction time decreased to the same extent as those of subjects who experienced the force field or sequence independently.     

Implicit motor learning from target error during explicit reach control

Many studies have shown adapted reaching in the face of altered visual feedback. These studies typically involve iterative corrections to the error induced by the perturbation until relatively normal performance is achieved. Here, we investigate whether adaptation (indexed by aftereffects) can occur when direct corrections to a target are inhibited by giving participants an explicit reach task. During the exposure phase of our study, participants were instructed to undershoot a target that imperceptibly moved between movement onset and movement end. The size of the target displacement was gradually increased, while the instructed undershoot distance was equivalently increased, such that participants were, unknowingly, aiming to the same location throughout exposure. When participants were subsequently instructed to aim at the target during the post-test, they overshot the target, suggesting that adaptation had occurred in the presence of an explicit task and in the absence of direct corrections to the target perturbation.     

Reach adaptation to explicit vs. implicit target error

The adaptation of reaching movements has typically been investigated by either distorting visual feedback of the reaching limb or by distorting the forces acting upon the reaching limb. Here, we investigate reach adaptation when error is created by systematically perturbing the target of the reach rather than the limb itself (Magescas and Prablanc in J Cogn Neurosci 18: 75–83, 2006). Specifically, we investigate how adaptation is affected by (1) the timing of the perturbation with respect to the movement of the eye and the hand and (2) participant awareness of the perturbation. In Experiment 1, participants looked and pointed to a target that disappeared either at the onset of their eye movement or shortly after their eye movement and then reappeared, displaced to the right, at the completion of the reach. In Experiment 2, we made the target displacement more explicit by leaving the target at its initial location until the end of the reach, at which point it was displaced to the right. In Experiment 3, we extinguished the target at the onset of the eye movement but also informed participants about the presence and magnitude of the perturbation. In the no-feedback post-test phase, participants for whom the target disappeared during the reach demonstrated much stronger aftereffects of the perturbation, misreaching to the right, whereas participants for whom the target stayed on until reach completion demonstrated rapid extinction of rightward misreaching. Furthermore, participants who were informed about the target perturbation exhibited faster de-adaptation than those who were not. Our results suggest that adaptation to a target displacement is contingent on the explicitness of the target perturbation, whether this is achieved by manipulating stimulus timing or instruction.     

Cross talk in implicit assignment of error information during bimanual visuomotor learning

When a neural movement controller, called an "internal model," is adapted to a novel environment, the movement error needs to be appropriately associated with the controller. However, their association is not necessarily guaranteed for bimanual movements in which two controllers--one for each hand--result in two movement errors. Considering the implicit nature of the adaptation process, the movement error of one hand can be erroneously associated with the controller of the other hand. Here, we investigated this credit-assignment problem in bimanual movement by having participants perform bimanual, symmetric back-and-forth movements while displaying the position of the right hand only with a cursor. In the training session, the cursor position was gradually rotated clockwise, such that the participants were unaware of the rotation. The movement of the right hand gradually rotated counterclockwise as a consequence of adaptation. Although the participants knew that the cursor reflected the movement of the right hand, such gradual adaptation was also observed for the invisible left hand, especially when the cursor was presented on the left side of the display. Thus the movement error of the right hand was implicitly assigned to the left-hand controller. Such cross talk in credit assignment might influence motor adaptation performance, even when two cursors are presented; the adaptation was impaired when the rotations imposed on the cursors were opposite compared with when they were in the same direction. These results indicate the inherent presence of cross talk in the process of associating action with consequence in bimanual movement.     

A spatial explicit strategy reduces error but interferes with sensorimotor adaptation

Although sensorimotor adaptation is typically thought of as an implicit form of learning, it has been shown that participants who gain explicit awareness of the nature of the perturbation during adaptation exhibit more learning than those who do not. With rare exceptions, however, explicit awareness is typically polled at the end of the study. Here, we provided participants with either an explicit spatial strategy or no instructions before learning. Early in learning, explicit instructions greatly reduced movement errors but also resulted in increased trial-to-trial variability and longer reaction times. Late in adaptation, performance was indistinguishable between the explicit and implicit groups, but the mechanisms underlying performance improvements remained fundamentally different, as revealed by catch trials. The progression of implicit recalibration in the explicit group was modulated by the use of an explicit strategy: these participants showed a lower level of recalibration as well as decreased aftereffects. This phenomenon may be due to the reduced magnitude of errors made to the target during adaptation or inhibition of implicit learning mechanisms by explicit processing.     

Age-related dedifferentiation of learning systems: an fMRI study of implicit and explicit learning

Abundant research finds that in young adults explicit learning (EL) is more dependent on the medial temporal lobes (MTL) whereas implicit learning (IL) is more dependent on the striatum. Using fMRI, we investigated age differences in each task and whether this differentiation is preserved in older adults. Results indicated that, while young recruited the MTL for EL and striatum for IL, both activations were significantly reduced in older adults. Additionally, results indicated that older adults recruited the MTL for IL, and this activation was significantly greater in older compared with young adults. A significant Task × Age interaction was found in both regions—with young preferentially recruiting the MTL for EL and striatum for IL, and older adults showing no preferential recruit for either task. Finally, young adults demonstrated significant negative correlations between activity in the striatum and MTL during both the EL and IL tasks. These correlations were attenuated in older adults. Taken together results support dedifferentiation in aging across memory systems.     

An ERP analysis of implicit structured sequence learning

When task exposure facilitates performance without producing corresponding changes in verbalizable knowledge, learning is said to be implicit. In Experiment I, event-related potentials (ERPs) were recorded as individuals practiced an implicit structured sequence learning (ISSL) task wherein only some target events required a response. With practice, the ERPs to targets that obeyed the underlying grammar diverged from those that did not at around 200 ms; grammatical targets appeared to be more positive between 200 and 500 ms because a similar positivity for the ungrammatical targets was delayed. In Experiment 2, the grammar was simplified allowing a direct comparison to be made between an implicit learning group and an explicit group, who were taught the grammar prior to recording. The results of the comparison revealed a remarkable similarity but did implicate at least partially nonidentical neural mechanisms in implicit and explicit strured sequence learning.     

Prefrontal lesions impair the implicit and explicit learning of sequences on visuomotor tasks

OBJECTIVE: (1) To verify whether the prefrontal cortex (PFC) is specifically involved in visuomotor sequence learning as opposed to other forms of motor learning and (2) to establish the role of executive functions in visuomotor sequence learning. BACKGROUND: Visuomotor skill learning depends on the integrity of the premotor and parietal cortex; the prefrontal cortex, however, is essential when the learning of a sequence is required. METHODS: We studied 25 patients with PFC lesions and 86 controls matched for age and educational level. Participants performed: (1) a Pursuit Tracking Task (PTT), composed of a random tracking task (perceptual learning) and a pattern tracking task (explicit motor sequence learning with learning indicated by the decrease in mean root square error across trial blocks), (2) a 12-item sequence version of a serial reaction time task (SRTT) with specific implicit motor sequence learning indicated by the rebound increase in response time when comparing the last sequence block with the next random block, and (3) a neuropsychological battery that assessed executive functions. RESULTS: PFC patients were impaired in sequence learning on the pattern tracking task of the PTT and on the SRTT as compared to controls, but performed normally on the PTT random tracking task. Learning on the PTT did not correlate with learning on the SRTT. PTT performance correlated with planning functions while SRTT performance correlated with working memory capacity. CONCLUSIONS: The PFC is specifically involved in explicit and implicit motor sequence learning. Different PFC regions may be selectively involved in such learning depending on the cognitive demands of the sequential task.     

A developmental study of event-related potentials during explicit and implicit memory

Event-related potentials (ERPs) were recorded from children, adolescents and adults in response to drawings of common objects or their printed names. Explicit memory was assessed in a continuous recognition paradigm, where each item had (old) or had not (new) been presented earlier. Implicit memory was assessed in separate blocks of pictures and words where item repetition was incidental to the assigned task of identifying stimuli in a given semantic category. Accuracy measures replicated the finding that word memory decays more rapidly than picture memory. A larger anterior negativity to pictures than words in children, but not adolescents or adults, suggested the existence of separate picture/word processing mechanisms that undergo developmental change. ERP repetition effects involved at least two components: a negativity that was larger to new items in both tasks, and a subsequent centroparietal positivity, most likely P3b, that was larger in response to old items for the explicit task only. Both components did not appear to undergo developmental change.     

Neural correlates of encoding and expression in implicit sequence learning

It has been shown that high-frequency repetitive transcranial magnetic stimulation (rTMS) to the human primary motor hand area (M1-HAND) can induce a lasting increase in corticospinal excitability. Here we recorded motor evoked potentials (MEPs) from the right first dorsal interosseus muscle to investigate how sub-threshold high-frequency rTMS to the M1-HAND modulates cortical and spinal excitability. In a first experiment, we gave 1500 stimuli of 5 Hz rTMS. At an intensity of 90% of active motor threshold, rTMS produced no effect on MEP amplitude at rest. Increasing the intensity to 90% of resting motor threshold (RMT), rTMS produced an increase in MEP amplitude. This facilitatory effect gradually built up during the course of rTMS, reaching significance after the administration of 900 stimuli. In a second experiment, MEPs were elicited during tonic contraction using weak anodal electrical or magnetic test stimuli. 1500 (but not 600) conditioning stimuli at 90% of RMT induced a facilitation of MEPs in the contracting FDI muscle. In a third experiment, 600 conditioning stimuli were given at 90% of RMT to the M1-HAND. Using two well-established conditioning-test paradigms, we found a decrease in short-latency intracortical inhibition (SICI), and a facilitation of the first peak of facilitatory I-waves interaction (SICF). There was no correlation between the relative changes in SICI and SICF. These results demonstrate that subthreshold 5 Hz rTMS can induce lasting changes in specific neuronal subpopulations in the human corticospinal motor system, depending on the intensity and duration of rTMS. Short 5 Hz rTMS (600 stimuli) at 90% of RMT can selectively shape the excitability of distinct intracortical circuits, whereas prolonged 5 Hz rTMS (900 stimuli) provokes an overall increase in excitability of the corticospinal output system, including spinal motoneurones.     

Event-related delta and theta synchronization during explicit and implicit emotion processing

Emotion information processing may occur in two modes which are differently represented in conscious awareness. Fast online processing involves coarse-grained analysis of salient features, and is not represented in conscious awareness; offline processing takes hundreds of milliseconds to generate fine-grained analysis, and is represented in conscious awareness. These processing modes may be studied using event-related electroencephalogram theta and delta synchronization as a marker of emotion processing. Two experiments were conducted, which differed on the mode of emotional information presentation. In the explicit mode subjects were explicitly instructed to evaluate the emotional content of presented stimuli; in the implicit mode they performed a gender discrimination task. Firstly, we show that in both experiments theta and delta synchronization is stronger upon presentation of “emotional” than “neutral” stimuli, and in subjects who are more sensitive, or experience higher emotional involvement than in less sensitive or detached subjects. Secondly, we show that in the implicit mode theta and delta synchronization is more pronounced in an early (before 250 ms post-stimulus) processing stage, whereas in the explicit mode it is more pronounced in a later processing stage. Source localization analysis showed that implicit processing of angry and happy (relative to neutral) faces is associated with higher early (before 250 ms) theta synchronization in the right parietal cortex and the right insula, respectively. Explicit processing of angry and happy faces is associated with higher late (after 250 ms) theta synchronization in the left temporal lobe and bilateral prefrontal cortex, respectively.     

Interactions between human explicit and implicit perceptual motor learning shown by kinematic variables

The goal of this study was to investigate in non-impaired humans the interaction between explicit and implicit learning in a catching task. The situation presented probabilistic contingencies between visual signals and various final pathways of the target. Subjects were asked to practice the interception task for 320 trials. Explicit instructions describing the probabilistic rules were given prior to (11 subjects), or in the middle of (11 subjects), physical practice. Eleven subjects not provided with verbal instructions served as control subjects. We measured the combination between explicit verbal instructions and implicit learning via kinematics of the end-effector and an outcome measure (i.e. spatial error). The time when explicit instructions were given resulted in systematic changes in the spatio-temporal ordering of the action. These data suggested that analyzing the way the task is executed with scrutiny allows a new understanding of how the aforementioned learning systems interact.     

The neural correlates of implicit sequence learning in schizophrenia

Twenty-seven schizophrenia spectrum patients and 25 healthy controls performed a probabilistic version of the serial reaction time task (SRT) that included sequence trials embedded within random trials. Patients showed diminished, yet measurable, sequence learning. Postexperimental analyses revealed that a group of patients performed above chance when generating short spans of the sequence. This high-generation group showed SRT learning that was similar in magnitude to that of controls. Their learning was evident from the very 1st block; however, unlike controls, learning did not develop further with continued testing. A subset of 12 patients and 11 controls performed the SRT in conjunction with positron emission tomography. High-generation performance, which corresponded to SRT learning in patients, correlated to activity in the premotor cortex and parahippocampus. These areas have been associated with stimulus-driven visuospatial processing. Taken together, these results suggest that a subset of patients who showed moderate success on the SRT used an explicit stimulus-driven strategy to process the sequential stimuli. This adaptive strategy facilitated sequence learning but may have interfered with conventional implicit learning of the overall stimulus pattern.     

Effects of priming goal pursuit on implicit sequence learning

Implicit learning, the type of learning that occurs without intent to learn or awareness of what has been learned, has been thought to be insensitive to the effects of priming, but recent studies suggest this is not the case. One study found that learning in the serial reaction time (SRT) task was improved by nonconscious goal pursuit, primed via a word search task (Eitam et al. in Psychol Sci 19:261–267, 2008). In two studies, we used the goal priming word search task from Eitam et al., but with a different version of the SRT, the alternating serial reaction time task (ASRT). Unlike the SRT, which often results in explicit knowledge and assesses sequence learning at one point in time, the ASRT has been shown to be implicit through sensitive measures of judgment, and it enables sequence learning to be measured continuously. In both studies, we found that implicit learning was superior in the groups that were primed for goal achievement compared to control groups, but the effect was transient. We discuss possible reasons for the observed time course of the positive effects of goal priming, as well as some future areas of investigation to better understand the mechanisms that underlie this effect, which could lead to methods to prolong the positive effects.     

Dissociable effects of the implicit and explicit memory systems on learning control of reaching

Adaptive control of reaching depends on internal models that associate states in which the limb experienced a force perturbation with motor commands that can compensate for it. Limb state can be sensed via both vision and proprioception. However, adaptation of reaching in novel dynamics results in generalization in the intrinsic coordinates of the limb, suggesting that the proprioceptive states in which the limb was perturbed dominate representation of limb state. To test this hypothesis, we considered a task where position of the hand during a reach was correlated with patterns of force perturbation. This correlation could be sensed via vision, proprioception, or both. As predicted, when the correlations could be sensed only via proprioception, learning was significantly better as compared to when the correlations could only be sensed through vision. We found that learning with visual correlations resulted in subjects who could verbally describe the patterns of perturbations but this awareness was never observed in subjects who learned the task with only proprioceptive correlations. We manipulated the relative values of the visual and proprioceptive parameters and found that the probability of becoming aware strongly depended on the correlations that subjects could visually observe. In all conditions, aware subjects demonstrated a small but significant advantage in their ability to adapt their motor commands. Proprioceptive correlations produced an internal model that strongly influenced reaching performance yet did not lead to awareness. Visual correlations strongly increased the probability of becoming aware, yet had a much smaller but still significant effect on reaching performance. Therefore, practice resulted in acquisition of both implicit and explicit internal models.     

Disentangling perceptual from motor implicit sequence learning with a serial color-matching task

This paper contributes to the domain of implicit sequence learning by presenting a new version of the serial reaction time (SRT) task that allows unambiguously separating perceptual from motor learning. Participants matched the colors of three small squares with the color of a subsequently presented large target square. An identical sequential structure was tied to the colors of the target square (perceptual version, Experiment 1) or to the manual responses (motor version, Experiment 2). Short blocks of sequenced and randomized trials alternated and hence provided a continuous monitoring of the learning process. Reaction time measurements demonstrated clear evidence of independently learning perceptual and motor serial information, though revealed different time courses between both learning processes. No explicit awareness of the serial structure was needed for either of the two types of learning to occur. The paradigm introduced in this paper evidenced that perceptual learning can occur with SRT measurements and opens important perspectives for future imaging studies to answer the ongoing question, which brain areas are involved in the implicit learning of modality specific (motor vs. perceptual) or general serial order.     

Intact implicit probabilistic sequence learning in obstructive sleep apnea

Obstructive sleep apnea (OSA) belongs to the sleep-related breathing disorders and is associated with cognitive impairments in learning and memory functions. The impairments in attention-demanding cognitive functions such as working memory and executive functions are well established in OSA; however, it remains unknown if less attention-demanding implicit sequence learning is affected. In the present study, we examined implicit sequence learning in OSA to probe the functional integrity of this fundamental learning mechanism. We used listening span to measure complex working memory capacity and the alternating serial reaction time (ASRT) task, which enables us to measure general skill learning and sequence-specific learning separately. Twenty OSA patients and 20 healthy controls participated in this study. Our data show dissociation between working memory and implicit sequence learning in OSA. Surprisingly, OSA patients showed preserved general skill and sequence-specific learning in spite of the possible hypoxia and sleep restriction. In contrast, working memory performance measured by listening span task was impaired in the OSA group. This finding suggests selective susceptibility of more attention-demanding cognitive functions in this patient population, while implicit learning remains intact. Our findings draw attention the fact that disordered sleep may have less impact on the integrity of structures connected to implicit sequence learning.