Impaired sequential and partially compensated probabilistic skill learning in Parkinson's disease

The striatal dopaminergic dysfunction in Parkinson's disease (PD) has been associated with deficits in skill learning in numerous studies, but some of the findings remain controversial. Our aim was to explore the generality of the learning deficit using two widely reported skill learning tasks in the same group of Parkinson's patients. Thirty-four patients with PD (mean age: 62.83 years, SD: 7.67) were compared to age-matched healthy adults. Two tasks were employed: the Serial Reaction Time Task (SRT), testing the learning of motor sequences, and the Weather Prediction (WP) task, testing non-sequential probabilistic category learning. On the SRT task, patients with PD showed no significant evidence for sequence learning. These results support and also extend previous findings, suggesting that motor skill learning is vulnerable in PD. On the WP task, the PD group showed the same amount of learning as controls, but they exploited qualitatively different strategies in predicting the target categories. While controls typically combined probabilities from multiple predicting cues, patients with PD instead focused on individual cues. We also found moderate to high correlations between the different measures of skill learning. These findings support our hypothesis that skill learning is generally impaired in PD, and can in some cases be compensated by relying on alternative learning strategies.     

Impaired skill learning in patients with severe closed-head injury as demonstrated by the serial reaction time (SRT) task

A group of 20 patients who sustained closed-head injury (CHI) and a matched control group of 20 individuals were tested on the serial reaction time (SRT) task. Three different sequence-learning measures were generated from the task: two implicit and one explicit. The two implicit sequence-learning measures include: (1) the learning rate on the first five blocks of the repeated sequence, assumed to reflect primarily general reaction time learning, and (2) the difference between the fifth block of the repeated sequence and the sixth block, a random sequence that reflects implicit sequence-specific learning. In addition, an explicit measure of sequence learning was generated. The results indicate that the CHI group was impaired on the explicit measure of sequence learning. The groups did not differ on general reaction time learning, one of the implicit measures of sequence learning. However, the control group was superior to the CHI group in learning the specific sequence repeated in the SRT task. This pattern of results is unique to the CHI group, corresponding with neither that of amnesic patients nor with that of patients with dysfunction of the basal ganglia (i.e., Parkinson's diseases).     

Sequence learning in Parkinson's disease: the effect of spatial stimulus-response compatibility

Patients with Parkinson's disease (PD) have repeatedly demonstrated reduced sequence-specific learning effects in serial reaction time tasks (SRTs). Previous research with PD patients has mainly employed the 'classical' SRT task, involving a spatially compatible assignment of stimuli and responses. From cognitive research, it is known that spatial compatibility triggers rapid, automatic responses in the direction of the stimulus. Automatic responding has shown to be disinhibited in PD patients and may therefore interfere with stimulus anticipation during the learning process. The aim of the present study was to test this hypothesis by investigating if reduced sequence-specific learning depends on spatial stimulus-response compatibility. PD patients and age-matched controls were examined either with an SRT variant involving central stimulus presentation, thereby preventing automatic linking of stimulus and response locations, or with a spatially compatible SRT task. Patients showed reduced sequence-specific learning effects only when the stimulus-response assignment was spatially compatible. This pattern of results confirms the hypothesis that sequence learning deficits in PD may result from a predominance of automatic response activation over learning-based stimulus anticipations during the learning phase.     

Specific sequence effects in the serial reaction time task

The Serial Reaction Time (SRT) task was used in 2 experiments to determine if the specific sequence used by the task influences implicit learning. In Experiment 1, participants performed the SRT task with the locations of the stimuli determined by a commonly used fixed sequence (taken from P. J. Reber & L. R. Squire, 1998), by a fixed sequence that was uniquely generated for each participant, or at random. Experiment 2 used the same basic design, but the random condition was changed so that each possible transition between responses was seen the same number of times, making it more comparable to the fixed-sequence conditions. Results from both experiments indicate that the specific sequence used in the SRT task influences the strength of implicit learning effects. Follow-up analyses show that the strength of implicit learning can be linked to the presence of particular types of triads within the sequence. The authors suggest that future researchers should not use on a single fixed sequence across all participants when using the SRT task but should instead generate different fixed sequences for each participant to enhance the generalizability of their results.     

Generalized lessons about sequence learning from the study of the serial reaction time task

Over the last 20 years researchers have used the serial reaction time (SRT) task to investigate the nature of spatial sequence learning. They have used the task to identify the locus of spatial sequence learning, identify situations that enhance and those that impair learning, and identify the important cognitive processes that facilitate this type of learning. Although controversies remain, the SRT task has been integral in enhancing our understanding of implicit sequence learning. It is important, however, to ask what, if anything, the discoveries made using the SRT task tell us about implicit learning more generally. This review analyzes the state of the current spatial SRT sequence learning literature highlighting the stimulus-response rule hypothesis of sequence learning which we believe provides a unifying account of discrepant SRT data. It also challenges researchers to use the vast body of knowledge acquired with the SRT task to understand other implicit learning literatures too often ignored in the context of this particular task. This broad perspective will make it possible to identify congruences among data acquired using various different tasks that will allow us to generalize about the nature of implicit learning.     

Manipulating attentional load in sequence learning through random number generation

Implicit learning is often assumed to be an effortless process. However, some artificial grammar learning and sequence learning studies using dual tasks seem to suggest that attention is essential for implicit learning to occur. This discrepancy probably results from the specific type of secondary task that is used. Different secondary tasks may engage attentional resources differently and therefore may bias performance on the primary task in different ways. Here, we used a random number generation (RNG) task, which may allow for a closer monitoring of a participant's engagement in a secondary task than the popular secondary task in sequence learning studies: tone counting (TC). In the first two experiments, we investigated the interference associated with performing RNG concurrently with a serial reaction time (SRT) task. In a third experiment, we compared the effects of RNG and TC. In all three experiments, we directly evaluated participants' knowledge of the sequence with a subsequent sequence generation task. Sequence learning was consistently observed in all experiments, but was impaired under dual-task conditions. Most importantly, our data suggest that RNG is more demanding and impairs learning to a greater extent than TC. Nevertheless, we failed to observe effects of the secondary task in subsequent sequence generation. Our studies indicate that RNG is a promising task to explore the involvement of attention in the SRT task.     

Does implicit learning in non-demented Parkinson’s disease depend on the level of cognitive functioning?

We investigated the influence of the level of cognitive functioning on sequence-specific learning in Parkinson's disease (PD). This was done by examining the relationship between the scales for outcomes in Parkinson's disease-cognition [SCOPA-COG, Marinus, J., Visser, M., Verwey, N. A., Verhey, F. R. J., Middelkoop, H. A. M.,Stiggelbout, A., et al. (2003). Assessment of cognition in Parkinson's disease. Neurology, 61, 1222-1228] and the serial reaction time (SRT) task [Nissen, M. J., & Bullemer, P. T. (1987). Attentional requirements for learning: Evidence from performance measures. Cognitive Psychology, 19, 1-32] in a homogeneous sample, consisting of 25 PD patients diagnosed in Stage 3 of the Hoehn and Yahr [Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: onset, progression, and mortality. Neurology, 17, 427-442] scale. Six patients in the low scoring cognitive group, 11 patients in the average scoring and eight patients in the high scoring group, conducted a SRT task with a deterministic sequence. Sequence-specific learning was assessed by inserting a random block to determine whether the acquisition of sequence movements differed between groups. Our results indicate an association between cognitive functioning in PD patients and sequence learning. These findings emphasize the use of assessing cognition in addition to the well-known motor aspects in PD.     

Is implicit sequence learning impaired in schizophrenia? A meta-analysis

Cognition in schizophrenia seems to be characterized by impaired performance on most tests of explicit or declarative learning contrasting with relatively intact performance on most tests of implicit or procedural learning. At the same time there have been conflicting results for studies that have used the Serial Reaction Time (SRT) task to examine implicit learning in people with schizophrenia. In the present research, we used meta-analysis to clarify whether or not people with schizophrenia show impaired performance on the SRT task. A systematic review found nine studies published in peer review journals that had each compared the performance of a group of people with schizophrenia with healthy controls on the standard SRT task or a variant of it. The resulting meta-analysis represented the responses of 205 participants with schizophrenia and 159 healthy controls on the SRT task. The analysis found that participants with schizophrenia perform less well than controls reflected by a pooled effect size of 0.51. A secondary analysis of all nine studies found that they all reported a point estimate of the change in reaction time between sequence and random trials that was greater for the controls. We conclude that there is a moderate impairment in implicit sequence learning among people with schizophrenia and speculate on the implications of this for understanding this disorder. Suggestions for improving the methodological quality and statistical reporting of studies of this topic are made.     

Attentional load and implicit sequence learning

A widely employed conceptualization of implicit learning hypothesizes that it makes minimal demands on attentional resources. This conjecture was investigated by comparing learning under single-task and dual-task conditions in the sequential reaction time (SRT) task. Participants learned probabilistic sequences, with dual-task participants additionally having to perform a counting task using stimuli that were targets in the SRT display. Both groups were then tested for sequence knowledge under single-task (Experiments 1 and 2) or dual-task (Experiment 3) conditions. Participants also completed a free generation task (Experiments 2 and 3) under inclusion or exclusion conditions to determine if sequence knowledge was conscious or unconscious in terms of its access to intentional control. The experiments revealed that the secondary task impaired sequence learning and that sequence knowledge was consciously accessible. These findings disconfirm both the notion that implicit learning is able to proceed normally under conditions of divided attention, and that the acquired knowledge is inaccessible to consciousness. A unitary framework for conceptualizing implicit and explicit learning is proposed.     

Sequence learning and selection difficulty

The authors studied the role of attention as a selection mechanism in implicit learning by examining the effect on primary sequence learning of performing a demanding target-selection task. Participants were trained on probabilistic sequences in a novel version of the serial reaction time (SRT) task, with dual- and triple-stimulus participants having to ignore irrelevant items in the SRT display. Despite large performance decrements under dual- and triple-stimulus configurations, testing under single-stimulus conditions revealed no impairment to sequence learning. These findings suggest that implicit sequence learning is resistant to disruption of the selection process. Results are discussed in terms of a componential model of attention and in relation to the implicit-explicit distinction.     

内隐序列学习不受注意负荷的影响:来自眼动的证据

利用眼动记录方法,采用内隐序列学习的观察范式,通过操纵注意负荷高和低,考察内隐序列学习是否需要注意参与。结果发现:(1)在高、低注意负荷条件下都出现了内隐序列学习效应;(2)高注意负荷条件下眼跳反应时长于低注意负荷条件下的;(3)高、低注意负荷序列内隐序列学习量差异不显著,表明内隐序列学习不受注意负荷影响。     

Anticipation measures of sequence learning: manual versus oculomotor versions of the serial reaction time task

The serial reaction time (SRT) task has generated a very large amount of research. Nevertheless the debate continues as to the exact cognitive processes underlying implicit sequence learning. Thus, the first goal of this study is to elucidate the underlying cognitive processes enabling sequence acquisition. We therefore compared reaction time (RT) in sequence learning in a standard manual activated (MA) to that in an ocular activated (OA) version of the task, within a single experimental setting. The second goal is to use eye movement measures to compare anticipation, as an additional indication of sequence learning, between the two versions of the SRT. Performance of the group given the MA version of the task (n = 29) was compared with that of the group given the OA version (n = 30). The results showed that although overall, RT was faster for the OA group, the rate of sequence learning was similar to that of the MA group performing the standard version of the SRT. Because the stimulus-response association is automatic and exists prior to training in the OA task, the decreased reaction time in this version of the task reflects a purer measure of the sequence learning that occurs in the SRT task. The results of this study show that eye tracking anticipation can be measured directly and can serve as a direct measure of sequence learning. Finally, using the OA version of the SRT to study sequence learning presents a significant methodological contribution by making sequence learning studies possible among populations that struggle to perform manual responses.     

Qualitative differences between implicit and explicit sequence learning

Four experiments investigate the differences between implicit and explicit sequence learning concerning their resilience to structural and superficial task changes. A superficial change that embedded the SRT task in the context of a selection task, while maintaining the sequence, did selectively hinder the expression of implicit learning. In contrast, a manipulation that maintained the task surface, but decreased the sequence validity, affected the expression of learning specifically when it was explicit. These results are discussed in the context of a dynamic framework (Cleeremans & Jiménez, 2002), which assumes that implicit knowledge is specially affected by contextual factors and that, as knowledge becomes explicit, it allows for the development of relevant metaknowledge that modulates the expression of explicit knowledge.     

Implicit Memory and the Formation of New Associations in Nondemented Parkinson′s Disease Individuals and Individuals with Senile Dementia of the Alzheimer Type: A Serial Reaction Time (SRT) Investigation

Using the serial reaction time (SRT) task developed by Nissen and Bullemer (1987, Cognitive Psychology, 19, 1–32), implicit memory performance was examined in four groups of subjects: nondemented healthy aged individuals; nondemented Parkinson"s disease individuals; very mildly demented senile dementia of the Alzheimer type (SDAT) individuals; and mildly demented SDAT individuals. The SRT task involved four blocks of a repeated 10-item keypress sequence that tapped general skill development along with a fifth block of a nonrepeated sequence that presumably reflected the impact of switching from a learned set of associations (developed during the first four blocks) to a novel sequence. The increase in response latency from the fourth repeated block to the fifth nonrepeated block was used as the reflection of implicit learning. The results revealed preserved implicit memory performance in the very mildly demented individuals compared to that of the age-matched control individuals. However, the mildly demented SDAT individuals and the nondemented Parkinson"s disease individuals showed reliably less implicit learning, compared to the age-matched control individuals. Differences between the past studies using the SRT task to tap implicit memory performance in SDAT individuals and the present study are discussed in some detail. We conclude that nondemented Parkinson"s disease individuals and mildly demented SDAT individuals produce some deficit in the formation of new associations in implicit memory, as measured by the SRT task.     

序列位置内隐学习产生机制的实验研究

内隐学习是当今认知和学习领域继内隐记忆之后又一重要的研究课题。该研究利用序列反应时研究程式,通过两个实验,对序列位置内隐学习产生的机制进行了探讨。结果表明：（１）在序列反应时任务程式中,随着反应一刺激间隔的延长,序列位置内隐学习的学习量逐渐减少;（２）异形同模式迁移组和异形异模式迁移组被试间内隐学习量无显著差异,被试未能内隐地习得抽象的序列模式。说明序列位置内隐学习产生的基础是水平联结,在该实验条件下没有发现垂直联结存在的证据。     

Impact of Parkinson’s disease and dopaminergic medication on adaptation to explicit and implicit visuomotor perturbations

The capacity to learn new visuomotor associations is fundamental to adaptive motor behavior. Evidence suggests visuomotor learning deficits in Parkinson’s disease (PD). However, the exact nature of these deficits and the ability of dopamine medication to improve them are under-explored. Previous studies suggested that learning driven by large and small movement errors engaged distinct neural mechanisms. Here, we investigated whether PD patients have a generalized impairment in visuomotor learning or selective deficits in learning from large explicit errors which engages cognitive strategies or small imperceptible movement errors involving primarily implicit learning processes. Visuomotor learning skills of non-medicated and medicated patients were assessed in two reaching tasks in which the size of visuospatial errors experienced during learning was manipulated using a novel three-dimensional virtual reality environment. In the explicit perturbation task, the visuomotor perturbation was applied suddenly resulting in large consciously detected initial spatial errors, whereas in the implicit perturbation task, the perturbation was gradually introduced in small undetectable steps such that subjects never experienced large movement errors. A major finding of this study was that PD patients in non-medicated and medicated conditions displayed slower learning rates and smaller adaptation magnitudes than healthy subjects in the explicit perturbation task, but performance similar to healthy controls in the implicit perturbation task. Also, non-medicated patients showed an average reduced deadaptation relative to healthy controls when exposed to the large errors produced by the sudden removal of the perturbation in both the explicit and implicit perturbation tasks. Although dopaminergic medication consistently improved motor signs, it produced a variable impact on learning the explicit perturbation and deadaptation and unexpectedly worsened performance in some patients. Considered together, these results indicate that PD selectively impairs the ability to learn from large consciously detected visuospatial errors. This finding suggests that basal ganglia-related circuits are important neural structures for adaptation to sudden perturbations requiring awareness and high-cost action selection. Dopaminergic treatment may selectively compromise the ability to learn from large explicit movement errors for reasons that remain to be elucidated.     

Social intuition as a form of implicit learning: Sequences of body movements are learned less explicitly than letter sequences

In the current paper, we first evaluate the suitability of traditional serial reaction time (SRT) and artificial grammar learning (AGL) experiments for measuring implicit learning of social signals. We then report the results of a novel sequence learning task which combines aspects of the SRT and AGL paradigms to meet our suggested criteria for how implicit learning experiments can be adapted to increase their relevance to situations of social intuition. The sequences followed standard finite-state grammars. Sequence learning and consciousness of acquired knowledge were compared between 2 groups of 24 participants viewing either sequences of individually presented letters or sequences of body-posture pictures, which were described as series of yoga movements. Participants in both conditions showed above-chance classification accuracy, indicating that sequence learning had occurred in both stimulus conditions. This shows that sequence learning can still be found when learning procedures reflect the characteristics of social intuition. Rule awareness was measured using trial-by-trial evaluation of decision strategy (Dienes & Scott, 2005; Scott & Dienes, 2008). For letters, sequence classification was best on trials where participants reported responding on the basis of explicit rules or memory, indicating some explicit learning in this condition. For body-posture, classification was not above chance on these types of trial, but instead showed a trend to be best on those trials where participants reported that their responses were based on intuition, familiarity, or random choice, suggesting that learning was more implicit. Results therefore indicate that the use of traditional stimuli in research on sequence learning might underestimate the extent to which learning is implicit in domains such as social learning, contributing to ongoing debate about levels of conscious awareness in implicit learning.     

Serial reaction time performance following right parietal lobe damage

The serial reaction time task (SRT) is used to assess implicit sequence learning. Neuroimaging studies implicate parietal involvement; however, the necessity of this area is unclear. We tested six unilateral right parietal patients and compared their performance to matched controls. Both groups showed similar levels of learning and explicit awareness. Two patients with the largest lesions extending into either frontal or cerebellar regions showed no learning. These data suggest that implicit sequence learning can occur despite damage to the right parietal lobe.     

What is the impact of the explicit knowledge of sequence regularities on both deterministic and probabilistic serial reaction time task performance?

The aim of this study was to explore the role of prior explicit sequence knowledge by comparing its influence on serial reaction time (SRT) performance with either a deterministic or a probabilistic sequence. The results confirm that, with a deterministic sequence, preliminary explicit learning improves SRT performance. On the other hand, with a probabilistic sequence, the results show no advantage for SRT performance in explicit-learning conditions. In addition, by using the process dissociation procedure (Jacoby, 1991), we show that performance on a subsequent generation task was more sustained by controlled processes for participants in the explicit-learning conditions than for those in the incidental condition. On the whole, these results, showing that the influence of explicit knowledge can be suppressed in certain specific conditions, are consistent with the intervention of both implicit and explicit mechanisms in SRT tasks, and the results also show that their relative influence can be modulated by the particular demands of the task.     

Sequence learning by action,observation and action observation

The serial reaction time (SRT) task was used to compare learning of a complex sequence by action (participants responded to sequential stimuli), by observation (participants watched but did not respond to sequential stimuli), and by action‐observation (participants watched an expert model responding to sequential stimuli). Each of these groups was compared with an untrained control group. Experiment 1 indicated that both observation and action‐observation were sufficient to support learning of a 12‐item second‐order conditional (SOC) sequence. Experiment 2 confirmed these findings, and showed that, as indexed by reaction time (RT), the extent of learning by observation and by action‐observation was comparable to that of action‐based learning. Using a recognition test, Experiment 2 and 3 also provided evidence that, whereas learning by stimulus observation was explicit, learning by action‐observation was implicit. These findings are consistent with a connection between motor systems and implicit learning, but do not support the hypothesis that overt action is necessary for implicit learning.