Phases of procedural learning and memory: characterisation with perceptual-motor sequence tasks

ABSTRACT

Procedural learning and memory has been conceptualised as consisting of cognitive and autonomous phases. Although the Serial Reaction Time Task (SRTT) is a popular task used to study procedural memory (PM), it has not been used to explore the different phases of PM. The present study employed a modified SRTT and investigated whether it can distinguish phases of PM. Our results revealed that performance at the beginning of typing a repeating sequence was marked by a steep learning curve, followed by gradual improvements and ending in high performance levels without further improvement. Steep performance increases characterise the effortful learning of the cognitive phase, gradual increases at higher performances characterise emerging automatisation of the associative phase, and sustained highest performance characterises autonomous procedures when PM has formed. Our study presents an easy-to-use measure, capable of distinguishing phases of PM, and which can be useful to assess PM during brain development.     

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.     

Pure perceptual-based learning of second-, third-, and fourth-order sequential probabilities

There is evidence that sequence learning in the traditional serial reaction time task (SRTT), where target location is the response dimension, and sequence learning in the perceptual SRTT, where target location is not the response dimension, are handled by different mechanisms. The ability of the latter mechanism to learn sequential contingencies that can be learned by the former mechanism was examined. Prior research has established that people can learn second-, third-, and fourth-order probabilities in the traditional SRTT. The present study reveals that people can learn such probabilities in the perceptual SRTT. This suggests that the two mechanisms may have similar architectures. A possible neural basis of the two mechanisms is discussed.     

Children's initial sleep‐associated changes in motor skill are unrelated to long‐term skill levels

Sleep is considered to support the formation of skill memory. In juvenile but not adult song birds learning a tutor's song, a stronger initial deterioration of song performance over night‐sleep predicts better song performance in the long run. This and similar observations have stimulated the view of sleep supporting skill formation during development in an unsupervised off‐line learning process that, in the absence of external feedback, can initially also enhance inaccuracies in skill performance. Here we explored whether in children learning a motor sequence task, as in song‐learning juvenile birds, changes across sleep after initial practice predict performance levels achieved in the long run. The task was a serial reaction time task (SRTT) where subjects had to press buttons which were lighted up in a repeating eight‐element sequence as fast as possible. Twenty‐five children (8–12 years) practised the task in the evening before nocturnal sleep which was recorded polysomnographically. Retrieval was tested on the following morning and again 1 week later after daily training on the SRTT. As expected, changes in response speed over the initial night of sleep were negatively correlated with final performance speed after the 1‐week training. However, unlike in song birds, this correlation was driven by the baseline speed level achieved before sleep. Baseline‐corrected changes in speed or variability over the initial sleep period did not predict final performance on the trained SRTT sequence, or on different sequences introduced to assess generalization of the trained behaviour. The lack of correlation between initial sleep‐dependent changes and long‐term performance might reflect that the children were too experienced for the simple SRTT, possibly also favouring ceiling effects in performance. A consistent association found between sleep spindle activity and explicit sequence knowledge alternatively suggests that the expected correlation was masked by explicit memory systems interacting with skill memory formation.     

Superstitious beliefs and the associative mind

Persistence of superstitions in the modern era could be justified by considering them as a by-product of the brain’s capacity to detect associations and make assumptions about cause-effect relationships. This ability, which supports predictive behaviour, directly relates to associative learning. We tested whether variability in superstitious behaviour reflects individual variability in the efficiency of mechanisms akin to habit learning. Forty-eight individuals performed a Serial Reaction Time Task (SRTT) or an Implicit Cuing Task (ICT). In the SRTT, participants were exposed to a hidden sequence and progressively learnt to optimize responses, a process akin to skill learning. In the ICT participants met with a hidden association, which (if detected) provided a benefit (cf. habit learning). An index of superstitious beliefs was also collected. A correlation emerged between susceptibility to personal superstitions and performance at the ICT only. This novel finding is discussed in view of current ideas on how superstitions are instated.     

左侧背外侧前额叶在程序性运动学习中的作用

程序性运动学习包括序列学习和随机学习。神经影像学研究表明背外侧前额叶皮层(DLPFC)和初级运动皮层(M1)在程序性运动学习中发挥重要作用, 但DLPFC和M1之间的联通性及其与不同程序性运动学习的关系尚不明确。本研究采用连续反应时间任务, 结合经颅磁刺激(TMS)方法, 探讨左侧DLPFC到M1的联通性在不同程序性运动学习中的差异。实验1采用两连发TMS探测DLPFC到M1的最佳投射时间点; 实验2, 被试分为2组, 分别进行序列学习和随机学习, 在学习前、后采集行为学数据, 以及M1的运动诱发电位和DLPFC-M1联通性的电生理学数据。行为学结果发现序列学习组的学习效果更佳; 电生理学结果发现, 两组被试学习前、后M1的运动诱发电位均未发生改变; 在最佳时间投射点、适当刺激强度下, 序列学习组DLPFC-M1联通性发生改变, 且与学习成绩相关, 而随机学习组没有改变。结果说明DLPFC到M1的联通性增强可能是序列学习成绩更佳的重要原因, 这一结果从电生理角度为DLPFC在运动学习中的作用提供了重要证据。     

Age-related differences in sequence learning: Findings from two visuo-motor sequence learning tasks

The Serial Reaction Time Task (SRTT) is thought to assess implicit learning, which seems to be preserved with age. However, the reaction time (RT) measures employed on implicit-like tasks might be too unreliable to detect individual differences. We investigated whether RT-based measures mask age effects by comparing the performance of 43 younger and 35 older adults on SRTT and an explicit-like Predictive Sequence Learning Task (PSLT). RT-based measures (difference scores and a ratio) were collected for both tasks, and accuracy was additionally measured for PSLT. We also measured fluid abilities. The RT-difference scores indicated preserved SRTT and PSLT performance with age and did not correlate with fluid abilities, while ratio RT and the accuracy-based measures indicated age-related decline and correlated with fluid abilities. Therefore, RT-difference scores might mask individual differences, which compromises the interpretation of previous studies using SRTT.     

基于脑结构像的精神分裂症机器学习分类

将机器学习应用于精神疾患的临床和基础研究是近年来的趋势。研究者将机器学习应用于精神分裂症患者及高危人群的T1加权像和弥散张量成像的脑影像数据中, 为了解疾病的生理病理学机制提供帮助。回顾以往研究发现额叶及颞叶的脑结构特征具有较高的区分能力, 行为数据和脑影像数据结合的分类效果优于单模态数据。现阶段研究存在样本量不足和泛化能力欠缺的局限, 未来研究应注意扩大样本量、制定标准化的分类方法, 从而进一步探究机器学习在精神疾患中的作用。     

The influence of focused-attention meditation states on the cognitive control of sequence learning

Cognitive control processes influence how motor sequence information is utilised and represented. Since cognitive control processes are shared amongst goal-oriented tasks, motor sequence learning and performance might be influenced by preceding cognitive tasks such as focused-attention meditation (FAM). Prior to a serial reaction time task (SRTT), participants completed either a single-session of FAM, a single-session of FAM followed by delay (FAM+) or no meditation (CONTROL). Relative to CONTROL, FAM benefitted performance in early, random-ordered blocks. However, across subsequent sequence learning blocks, FAM+ supported the highest levels of performance improvement resulting in superior performance at the end of the SRTT. Performance following FAM+ demonstrated greater reliance on embedded sequence structures than FAM. These findings illustrate that increased top-down control immediately after FAM biases the implementation of stimulus-based planning. Introduction of a delay following FAM relaxes top-down control allowing for implementation of response-based planning resulting in sequence learning benefits.     

Habit and skill learning in schizophrenia: evidence of normal striatal processing with abnormal cortical input

Different forms of nondeclarative learning involve regionally specific striatal circuits. The motor circuit (involving the putamen) has been associated with motor–skill learning and the dorsolateral prefrontal cortex (DLPFC) circuit (involving the caudate) has been associated with cognitive–habit learning. Efforts to differentiate functional striatal circuits within patient samples have been limited. Previous studies have provided mixed results regarding striatal-dependent nondeclarative learning deficits in patients with schizophrenia. In this study, a cognitive–habit learning task (probabilistic weather prediction) was used to assess the DLPFC circuit and a motor–skill learning task (pursuit rotor) was used to assess the motor circuit in 35 patients with schizophrenia and 35 normal controls. Patients with schizophrenia displayed significant performance differences from controls on both nondeclarative tasks; however, cognitive–habit learning rate in patients did not differ from controls. There were performance and learning-rate differences on the motor–skill learning task between the whole sample of patients and controls, however, analysis of a subset of patients and controls matched on general intellectual level eliminated learning rate differences between groups. The abnormal performance offset between patients with schizophrenia and controls in the absence of learning rate differences suggests that abnormal cortical processing provides altered input to normal striatal circuitry.     

Implicit learning of predictive relationships in three-element visual sequences by young and old adults

Knowledge of sequential relationships enables future events to be anticipated and processed efficiently. Research with the serial reaction time task (SRTT) has shown that sequence learning often occurs implicitly without effort or awareness. Here, the authors report 4 experiments that use a triplet-learning task (TLT) to investigate sequence learning in young and older adults. In the TLT, people respond only to the last target event in a series of discrete, 3-event sequences or triplets. Target predictability is manipulated by varying the triplet frequency (joint probability) and/or the statistical relationships (conditional probabilities) among events within the triplets. Results reveal that both groups learned, though older adults showed less learning of both joint and conditional probabilities. Young people used the statistical information in both cues, but older adults relied primarily on information in the 2nd cue alone. The authors conclude that the TLT complements and extends the SRTT and other tasks by offering flexibility in the kinds of sequential statistical regularities that may be studied as well as by controlling event timing and eliminating motor response sequencing.     

One-year retention of general and sequence-specific skills in a probabilistic,serial reaction time task

Procedural skills such as riding a bicycle and playing a musical instrument play a central role in daily life. Such skills are learned gradually and are retained throughout life. The present study investigated 1-year retention of procedural skill in a version of the widely used serial reaction time task (SRTT) in young and older motor-skill experts and older controls in two experiments. The young experts were college-age piano and action video-game players, and the older experts were piano players. Previous studies have reported sequence-specific skill retention in the SRTT as long as 2 weeks but not at 1 year. Results indicated that both young and older experts and older non-experts revealed sequence-specific skill retention after 1 year with some evidence that general motor skill was retained as well. These findings are consistent with theoretical accounts of procedural skill learning such as the procedural reinstatement theory as well as with previous studies of retention of other motor skills.     

Distorted estimates of implicit and explicit learning in applications of the process-dissociation procedure to the SRT task

We investigated potential biases affecting the validity of the process-dissociation (PD) procedure when applied to sequence learning. Participants were or were not exposed to a serial reaction time task (SRTT) with two types of pseudo-random materials. Afterwards, participants worked on a free or cued generation task under inclusion and exclusion instructions. Results showed that pre-experimental response tendencies, non-associative learning of location frequencies, and the usage of cue locations introduced bias to PD estimates. These biases may lead to erroneous conclusions regarding the presence of implicit and explicit knowledge. Potential remedies for these problems are discussed.     

Post–traumatic stress disorder in patients with coronary artery disease: A review and evaluation of the risk

Psychosocial factors are known to impact on the prognosis of patients with coronary artery disease independently of disease severity. However, few studies have looked at whether these patients are at risk of developing post-traumatic stress disorder, and the potential implications for morbidity and mortality. Through a review of the empirical literature, the objectives were to investigate whether patients with coronary artery disease are at risk of developing this disorder, to look at relations between post-traumatic stress disorder and heart disease, and to stimulate further research. The review indicated that some patients with coronary artery disease are at risk of developing post-traumatic stress disorder, although the prevalence varied considerably. Methodological issues together with recommendations for future research are discussed. Although only some cardiac patients may develop post-traumatic stress, this disorder should not be overlooked due to its potential role in reinfarctions and mortality.     

The MMPI‐2 in chronic psychiatric illness

While previous studies on the MMPI‐2 in patients with schizophrenia and depression have used mixed samples of both early stage and chronic psychiatric patients. Here, it is investigated whether chronicity itself might have a differential effect on the MMPI‐2 profiles of these patients and whether demoralization ‘associated with long‐term illness’ affects the scales of the MMPI‐2. Thirty long‐term patients with schizophrenia, 30 long‐term patients with depression, and 30 healthy participants completed the MMPI‐2. Groups were compared on Clinical Scales and on the Restructured Clinical (RC) Scales. Patients with schizophrenia differed from patients with depression on 14 MMPI‐2 scales and from healthy controls on 10 scales, generally showing mean UT‐scores < 65, indicating a subjective experience of (near) normal functioning. Patients with depression differed from healthy controls on 17 scales mostly with UT‐scores > 65, indicating impaired functioning. Demoralization was higher in patients with depression than in patients with schizophrenia and both psychiatric groups differed from the healthy control group. It is concluded that long‐term patients with depression show impaired functioning and high demoralization, while long‐term patients with schizophrenia surprisingly show near normal functioning and less demoralization.     

Brain abnormalities observed in childhood-onset schizophrenia: a review of the structural magnetic resonance imaging literature

Childhood-onset schizophrenia (COS) is a rare, severe form of schizophrenia in which there are structural brain abnormalities that may be related to the psychotic symptomatology and neurocognitive deficits found in these patients. While there are numerous structural imaging studies of the adult-onset variant of schizophrenia (with many conflicting findings), relatively few brain imaging studies of COS have been conducted. This paper summarizes the extant literature of magnetic resonance imaging (MRI) studies of structural brain abnormalities in COS, and compares findings to similar studies of adult-onset patients. Volumetric MRI studies of COS patients have consistently shown evidence for increased ventricular volume, reduced cerebral gray matter, and increased caudate volume, consistent with findings from adult-onset studies. Other volumetric brain abnormalities are observed in COS patients, such as reduced total brain volume, but not consistently across all studies. Voxel-based morphometric analyses have revealed abnormalities in the shape and spatial location of structures in COS such as the corpus callosum, caudate, and thalamus that could not be observed in the more traditional volumetric assessments. Similar findings also are observed in adult-onset patients. Progressive degenerative changes, such as ventricular enlargement, appear to occur in COS only until young adulthood where there is an apparent asymptote with no further degenerative changes. This is consistent with the lack of progressive changes noted in most longitudinal studies of adult-onset schizophrenia.     

睡眠对知觉与动作序列内隐学习离线巩固效应的影响

离线阶段发生的学习被称为离线巩固, 即在最初获得知识之后, 即使没有额外的练习, 其记忆痕迹也会保持稳定或提高。有研究初步探究了睡眠对知觉和动作序列内隐学习离线巩固的影响, 然而, 这些研究未能实现知觉序列与动作序列的完全分离, 序列类型是否调节睡眠对内隐序列学习离线巩固的影响仍需进一步探讨。此外, 既往外显学习的研究发现相对于简单的序列, 复杂的序列更容易从睡眠中获益, 表现出基于睡眠的离线巩固效应。睡眠对知觉序列与动作序列内隐学习离线巩固的影响是否会受到序列复杂程度的调节尚不明确。为此, 本研究在完全分离知觉序列和动作序列的情况下, 通过3个实验操纵序列的长度及结构, 设置3种不同复杂程度的序列规则, 考察了这一问题。结果发现, 对于动作序列, 序列规则复杂程度较低时, 无论是否经过睡眠都会发生离线巩固效应, 而当动作序列规则较为复杂时, 只有经历睡眠才会引起离线巩固效应; 对于知觉序列, 无论何种难易程度的规则, 均未发生离线巩固效应。上述结果表明内隐序列知识基于睡眠的离线巩固会受到序列类型及序列复杂程度的调节, 这为内隐学习的离线巩固争论提供了新的视角。     

Learning and forgetting in schizophrenia

Recent studies of patients with schizophrenia have consistently demonstrated marked deficits on measures of initial learning. However, contradictory results have been reported concerning retention and forgetting. The present study examined the level of initial and delayed recall of stories and visual figures in a group of 76 patients with schizophrenia and 51 normal controls. Schizophrenia patients demonstrated marked impairments in initial and delayed recall as well as significantly worse percentage retention scores. However, schizophrenia patients and healthy controls individually matched on level of initial recall had nearly identical delayed recall performance. The results suggest a primary deficit in the initial acquisition of information rather than an accelerated rate of forgetting in schizophrenia.     

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.     

Auditory sequence learning: differential sensitivity to task relevant and task irrelevant sequences

Using a serial reaction time task, this study examines whether learning of auditory sequences is possible without a corresponding motor response, i.e., by listening alone. The dual sequence paradigm used by Mayr (in Journal of the Experimental Psychology: Learning memory and cognition 22:350–354, 1996, Experiment 1) was adapted to the auditory domain. Four different actors spoke the same four colour words. These were presented such that speaker identity followed one sequence, and the word spoken followed a different sequence. Subjects were asked to respond (with a key press) to one of these dimensions (identity or word), and ignore the other. Results showed learning for either type of stimulus, but only when it was responded to. No learning of either type of auditory sequence by listening alone was found. The results add evidence to visual implicit learning studies that have failed to find learning of event sequences when spatial or response selection was not an important factor in processing. The findings are discussed in the context of implicit learning as a general and fundamental cognitive process.