The role of the basal ganglia in implicit contextual learning: A study of Parkinson's disease

Implicit contextual learning refers to the ability to memorize contextual information from our environment. This contextual information can then be used to guide our attention to a specific location. Although the medial temporal lobe is important for this type of learning, the basal ganglia might also be involved considering its role in many implicit learning processes. In order to understand the role of the basal ganglia in this top-down process, a group of non-demented early-stage Parkinson's patients were tested with a contextual cueing task. In this visual search task, subjects have to quickly locate a target among a number of distractors. To test implicit contextual learning, some of the configurations are repeated during the experiment, resulting in faster responses. A significant interaction effect was found between Group and Configuration, indicating that the control subjects responded faster when the spatial context was repeated, whereas Parkinson's patients failed to do so. These results, showing that the contextual cueing effect was significantly different for the patients than for the controls, suggest an important role for the basal ganglia in implicit contextual learning, thus extending previous findings of medial temporal lobe involvement. The basal ganglia are therefore not only involved in implicit motor learning, but may also have a role in purely visual implicit learning.     

The role of the basal ganglia and its cortical connections in sequence learning: Evidence from implicit and explicit sequence learning in Parkinson's disease

Implicit (unconscious/incidental) and explicit (conscious/intentional) learning are considered to have distinct neural substrates. It is proposed that implicit learning is mediated by the basal ganglia (BG), while explicit learning has been linked to the medial temporal lobes (MTL). To test such a dissociation we investigated implicit and explicit sequence learning in Parkinson's disease (PD), a disorder characterized by striatal dysfunction. We studied both implicit and explicit learning of a 12-item sequence of target locations in 13 PD patients and 15 age-matched controls. In the implicit sequence learning task all participants completed 10 blocks of a probabilistic serial reaction time (SRT) task in which they were exposed to the sequence without explicit knowledge of it. Participants also completed between 1 and 10 blocks of an explicit sequence learning task in which the sequence was learned deliberately by trial-and-error. Both implicit and explicit sequence learning were significantly impaired in PD patients compared to controls. The results indicate that, in addition to playing a role in implicit sequence learning, the BG and its frontal projections are also involved in explicit sequence learning.     

Intact implicit learning in schizophrenia

OBJECTIVE: Schizophrenia impairs performance on explicit, but not implicit, memory tasks, indicating that conscious awareness at retrieval is a critical determinant of impaired memory. The authors investigated implicit learning, i.e., knowledge acquisition in the absence of conscious awareness, in patients with schizophrenia. METHOD: An artificial grammar learning task was used to assess implicit learning in 48 patients with schizophrenia and 24 healthy comparison subjects. The subjects were first presented with letter strings that were generated according to the rules of a finite-state grammar paradigm. They were then required to indicate whether new letter strings were "grammatical," depending on whether or not the strings corresponded to the rules. IQ, working memory, explicit memory, verbal fluency, and speed of processing were also assessed. RESULTS: Patients performed significantly worse than the comparison subjects on cognitive tasks that assessed episodic memory, verbal fluency, working memory, and speed of processing. In contrast, patients classified as being correct more grammatical than nongrammatical letter strings, and the magnitude of the difference was similar to that observed in healthy comparison subjects. CONCLUSIONS: Implicit learning, as assessed with an artificial grammar learning task, is intact in patients with schizophrenia. Conscious awareness might be a critical determinant of memory impairment both at encoding and at retrieval.     

Learning of writing letter-like sequences in children with physical and multiple disabilities

This study compared implicit and explicit learning instructions in hand writing. Implicit learning is the ability to acquire a new skill without a corresponding increase in knowledge about the skill. In contrast, explicit learning uses declarative knowledge to build up a set of performance rules that guide motor performance or skills. Explicit learning is dependent on working memory, implicit learning is not. Therefore, implicit learning was expected to be easier than explicit learning in children in special education, given their expected compromised working memory. Two groups of children (5–12 years) participated, children in special education with physical or multiple disabilities (study group, n = 22), and typically developing controls (n = 32). Children learned to write letter-like patterns on a digitizer by tracking a moving target (implicitly) and verbal instruction (explicitly). We further tested visual working memory, visual-motor integration, and gross manual dexterity. Learning curves were similar for both groups in both conditions; children in the study group did learn both implicitly and explicitly. Motor performance was related to the writing task. In contrast to our hypothesis, visual working memory was not an important factor in the explicit condition. These results shed new light on the conceptual difference between implicit and explicit learning, and the role of working memory therein.     

A study of parallel implicit and explicit information processing in patients with obsessive-compulsive disorder

OBJECTIVE: This study examined implicit sequence learning in patients with obsessive-compulsive disorder (OCD) under dual-task conditions. Frontal-striatal networks support implicit learning and are implicated in the pathophysiology of OCD. Neuroimaging data suggest that during implicit learning, OCD patients use neural systems normally active during explicit learning to compensate for striatal dysfunction. METHOD: The authors examined implicit sequence learning in 25 OCD patients and 25 healthy comparison subjects using a dual-task paradigm, with subjects simultaneously engaged in an explicit memory task and an implicit learning task. They predicted that implicit learning in OCD subjects would be disrupted because concurrent explicit information-processing demands would prevent use of compensatory processes. RESULTS: OCD patients failed to show evidence of implicit learning and exhibited a significant deficit in comparison with healthy subjects. CONCLUSIONS: These results are consistent with the hypothesis that concurrent explicit and implicit information-processing demands interfere with implicit learning in OCD patients.     

A Single Paradigm for Implicit and Statistical Learning

Implicit learning generally refers to the acquisition of structures that, like knowledge of natural language grammar, are not available to awareness. In contrast, statistical learning has frequently been related to learning language structures that are explicitly available, such as vocabulary. In this paper, we report an experimental paradigm that enables testing of both classic implicit and statistical learning in language. The paradigm employs an artificial language comprising sentences that accompany visual scenes that they represent, thus combining artificial grammar learning with cross‐situational statistical learning of vocabulary. We show that this methodology enables a comparison between acquisition of grammar and vocabulary, and the influences on their learning. We show that both grammar and vocabulary are promoted by explicit information about the language structure, that awareness of structure affects acquisition during learning, and awareness precedes learning, but is not distinctive at the endpoint of learning. The two traditions of learning—implicit and statistical—can be conjoined in a single paradigm to explore both the phenomenological and learning consequences of statistical structural knowledge.     

Severity of explicit memory impairment due to Alzheimer’s disease improves effectiveness of implicit learning

Background Consistent evidence from human and experimental animals studies indicates that memory is organized into two relatively independent systems with different functions and brain mechanisms. The explicit memory system, dependent on the hippocampus and adjacent medial temporal lobe structures, refers to conscious knowledge acquisition and intentional recollection of previous experiences. The implicit memory system, dependent on the striatum, refers to learning of complex information without awareness or intention. The functioning of implicit memory can be observed in progressive, gradual improvement across many trials in performance on implicit learning tasks. The influence of explicit memory on implicit memory has not been precisely identified yet. According to data from some studies, explicit memory seems to exhibit no influence on implicit memory,whereas the other studies indicate that explicit memory may inhibit or facilitate implicit memory. Objectives The analysis of performance on implicit learning tasks in patients with different severity of explicit memory impairment due to Alzheimer’s disease allows one to identify the potential influence of the explicit memory system on the implicit memory system. Patients and methods 51 patients with explicit memory impairment due to Alzheimer’s disease (AD) and 36 healthy controls were tested. Explicit memory was examined by means of a battery of neuropsychological tests. Implicit habit learning was examined on probabilistic classification task (weather prediction task). Results Patients with moderate explicit memory impairment performed the implicit task significantly better than those with mild AD and controls. Conclusion Results of our study support the hypothesis of competition between the implicit and explicit memory systems in humans.     

Neural correlates of contextual cueing are modulated by explicit learning

Contextual cueing refers to the facilitated ability to locate a particular visual element in a scene due to prior exposure to the same scene. This facilitation is thought to reflect implicit learning, as it typically occurs without the observer's knowledge that scenes repeat. Unlike most other implicit learning effects, contextual cueing can be impaired following damage to the medial temporal lobe. Here we investigated neural correlates of contextual cueing and explicit scene memory in two participant groups. Only one group was explicitly instructed about scene repetition. Participants viewed a sequence of complex scenes that depicted a landscape with five abstract geometric objects. Superimposed on each object was a letter T or L rotated left or right by 90°. Participants responded according to the target letter (T) orientation. Responses were highly accurate for all scenes. Response speeds were faster for repeated versus novel scenes. The magnitude of this contextual cueing did not differ between the two groups. Also, in both groups repeated scenes yielded reduced hemodynamic activation compared with novel scenes in several regions involved in visual perception and attention, and reductions in some of these areas were correlated with response-time facilitation. In the group given instructions about scene repetition, recognition memory for scenes was superior and was accompanied by medial temporal and more anterior activation. Thus, strategic factors can promote explicit memorization of visual scene information, which appears to engage additional neural processing beyond what is required for implicit learning of object configurations and target locations in a scene.     

Patients with Parkinson's disease learn to control complex systems-an indication for intact implicit cognitive skill learning

Implicit memory and learning mechanisms are composed of multiple processes and systems. Previous studies demonstrated a basal ganglia involvement in purely cognitive tasks that form stimulus response habits by reinforcement learning such as implicit classification learning. We will test the basal ganglia influence on two cognitive implicit tasks previously described by Berry and Broadbent, the sugar production task and the personal interaction task. Furthermore, we will investigate the relationship between certain aspects of an executive dysfunction and implicit learning. To this end, we have tested 22 Parkinsonian patients and 22 age-matched controls on two implicit cognitive tasks, in which participants learned to control a complex system. They interacted with the system by choosing an input value and obtaining an output that was related in a complex manner to the input. The objective was to reach and maintain a specific target value across trials (dynamic system learning). The two tasks followed the same underlying complex rule but had different surface appearances. Subsequently, participants performed an executive test battery including the Stroop test, verbal fluency and the Wisconsin card sorting test (WCST). The results demonstrate intact implicit learning in patients, despite an executive dysfunction in the Parkinsonian group. They lead to the conclusion that the basal ganglia system affected in Parkinson's disease does not contribute to the implicit acquisition of a new cognitive skill. Furthermore, the Parkinsonian patients were able to reach a specific goal in an implicit learning context despite impaired goal directed behaviour in the WCST, a classic test of executive functions. These results demonstrate a functional independence of implicit cognitive skill learning and certain aspects of executive functions.     

Primary motor and premotor cortex in implicit sequence learning - evidence for competition between implicit and explicit human motor memory systems

Implicit and explicit memory systems for motor skills compete with each other during and after motor practice. Primary motor cortex (M1) is known to be engaged during implicit motor learning, while dorsal premotor cortex (PMd) is critical for explicit learning. To elucidate the neural substrates underlying the interaction between implicit and explicit memory systems, adults underwent a randomized crossover experiment of anodal transcranial direct current stimulation (AtDCS) applied over M1, PMd or sham stimulation during implicit motor sequence (serial reaction time task, SRTT) practice. We hypothesized that M1‐AtDCS during practice will enhance online performance and offline learning of the implicit motor sequence. In contrast, we also hypothesized that PMd‐AtDCS will attenuate performance and retention of the implicit motor sequence. Implicit sequence performance was assessed at baseline, at the end of acquisition (EoA), and 24 h after practice (retention test, RET). M1‐AtDCS during practice significantly improved practice performance and supported offline stabilization compared with Sham tDCS. Performance change from EoA to RET revealed that PMd‐AtDCS during practice attenuated offline stabilization compared with M1‐AtDCS and sham stimulation. The results support the role of M1 in implementing online performance gains and offline stabilization for implicit motor sequence learning. In contrast, enhancing the activity within explicit motor memory network nodes such as the PMd during practice may be detrimental to offline stabilization of the learned implicit motor sequence. These results support the notion of competition between implicit and explicit motor memory systems and identify underlying neural substrates that are engaged in this competition.     

Allocentric memory impaired and egocentric memory intact as assessed by virtual reality in recent-onset schizophrenia

Present evidence suggests that schizophrenia is associated with explicit memory deficits, whereas implicit memory seems to be largely preserved. Virtual reality studies on declarative allocentric memory in schizophrenia are rare, and studies on implicit egocentric memory in schizophrenia are lacking. However, virtual realities have a major advantage for the assessment of spatial navigation and memory formation, as computer-simulated first-person environments can simulate navigation in a large-scale space. Twenty-five subjects with recent-onset schizophrenia were compared with 25 healthy matched control subjects on two virtual reality tasks affording the navigation and learning of a virtual park (allocentric memory) and a virtual maze (egocentric memory). Compared with control subjects, schizophrenia subjects were significantly impaired in learning the virtual park. However, schizophrenia subjects were as able as control subjects to learn the virtual maze. Stronger disorganized symptoms of schizophrenia subjects were significantly related to more errors on the virtual maze. It is concluded that egocentric spatial learning adds to the many other implicit cognitive skills being largely preserved in schizophrenia. Possibly, the more global neural network supporting egocentric spatial learning is less affected than the declarative hippocampal memory system in early stages of schizophrenia and may offer opportunities for compensation in the presence of focal deficits.     

Implicit and explicit learning in young adults with mental retardation

We examined intelligence-related differences in explicit and implicit learning using an artificial grammar paradigm. Young adults with and without mental retardation completed a sequence-learning and identification task. For some participants, sequences were constructed following an artificial grammar; for others, sequences were random. Explicit learning was determined by ability to learn and later identify random sequences. Implicit learning was determined by the tendency to incorrectly identify new grammatical sequences as seen before, relative to new nongrammatical sequences. Participants with mental retardation did more poorly than participants without mental retardation on explicit learning but just as well on implicit learning. Results suggest that learning of complex materials, when accomplished through implicit processing, is functionally equivalent in individuals with and without mental retardation.     

Sparing of perceptual implicit memory despite suppression of the electrophysiological word repetition effect: a study with general anesthetic isoflurane.

OBJECTIVE: Much effort has been devoted to the search for the neurophysiological correlates of implicit memory. A commonly held view is that the early portion (250-500 ms) of the event-related potential (ERP) word repetition effect reflects processes important for perceptual implicit memory whereas the latter portion reflects processes implicated in explicit memory. It is, however, difficult to disentangle with certainty the relative contributions of each form of memory on ERPs since both forms co-exist in normal subjects. To dissociate ERP effect related to implicit and explicit memory, we used isoflurane sedation in normal subjects to suppress explicit remembering while sparing implicit memory. These ERPs were compared with those of non-medicated control subjects. METHODS: Thirteen subjects performed an incidental encoding task for words presented auditorily during the inhalation of a subanesthetic dose of isoflurane. After termination of isoflurane administration, we assessed free recall and recorded ERPs during a syllable completion task (implicit memory) and during a passive listening task (ERP repetition effect). Eleven non-medicated control subjects were tested in a similar manner. RESULTS: The controls showed robust early and late ERP repetition effect. The isoflurane group had implicit memory without free recall and showed no ERP repetition effect. CONCLUSIONS: These findings failed to show an association between any part of the repetition effect and perceptual implicit memory. The results are consistent with the view that processes linked to explicit memory contribute to the ERP repetition effect since there was a marked difference in free recall between the control and isoflurane groups. SIGNIFICANCE: The present study shows that the reversible alterations of memory by general anesthetics can be used to study the neurophysiological correlates of memory processes.     

Selective memory and memory deficits in depressed inpatients

We investigated memory impairment and mood-congruent memory bias in depression, using an explicit memory test and an implicit one. Thirty-six severely depressed inpatients that fulfilled DSM-IV criteria for major depressive disorder and 36 healthy controls matched for sex, age, and educational level participated in the study. Explicit memory was assessed with a free recall task and implicit memory with an anagram solution task. Results showed that depressed and controls differed in explicit memory performance, depending on the amount of cognitive distraction between incidental learning and testing. Implicit memory was not affected. In addition, severely depressed patients showed a mood-congruent memory bias in implicit memory but not in explicit memory. The complex pattern of results is discussed with regard to relevant theories of depression.     

Performing prototype distortion tasks requires no contribution from the explicit memory systems: Evidence from amnesic MCI patients in a new experimental paradigm

Evidence shows that amnesic patients are able to categorize new exemplars drawn from the same prototype as in previously encountered items. It is still unclear, however, whether this ability is due to a spared implicit learning system or residual explicit memory and/or working memory resources. In this study, we used a new paradigm devised expressly to rule out any possible contribution of episodic and working memory in performing a prototype distortion task.We enrolled patients with amnesic MCI and Normal Controls. Our paradigm consisted of a study phase and a test phase; two-thirds of the participants performed the study phase and all participants performed the test phase. In the study phase, participants had to judge how pleasant morphed faces, drawn from a single prototype, seemed to them. Half of the participants were shown faces drawn from the A-prototype and half from the B-prototype. A- and B-faces were opposite in a morphing space with a neutral human face at the center. In the test phase, participants had to judge the regularity of faces they had never seen before. Three different types of faces were shown in the test phase, that is, A-, B-, or neutral-faces. We expected that implicit learning of the category boundaries would lead to a category-specific increase in perceived regularity. The results confirmed our predictions. In fact, trained subjects (compared with subjects who did not undergo the study phase) assigned higher regularity scores to new faces drawn from the same prototype as the faces seen during training, and they gave lower regularity scores to new faces drawn from the opposite prototype. This effect was super imposable across subjects' groups.     

The metabotropic glutamate receptor,mGlu5, is required for extinction learning that occurs in the absence of a context change

The metabotropic glutamate (mGlu) receptors and, in particular, mGlu5 are crucially involved in multiple forms of synaptic plasticity that are believed to underlie explicit memory. MGlu5 is also required for information transfer through neuronal oscillations and for spatial memory. Furthermore, mGlu5 is involved in extinction of implicit forms of learning. This places this receptor in a unique position with regard to information encoding. Here, we explored the role of this receptor in context‐dependent extinction learning under constant, or changed, contextual conditions. Animals were trained over 3 days to take a left turn under 25% reward probability in a T‐maze with a distinct floor pattern (Context A). On Day 4, they experienced either a floor pattern change (Context B) or the same floor pattern (Context A) in the absence of reward. After acquisition of the task, the animals were returned to the maze once more on Day 5 (Context A, no reward). Treatment with the mGlu5 antagonist, 2‐methyl‐6‐(phenylethynyl) pyridine, before maze exposure on Day 4 completely inhibited extinction learning in the AAA paradigm but had no effect in the ABA paradigm. A subsequent return to the original context (A, on Day 5) revealed successful extinction in the AAA paradigm, but impairment of extinction in the ABA paradigm. These data support that although extinction learning in a new context is unaffected by mGlu5 antagonism, extinction of the consolidated context is impaired. This suggests that mGlu5 is intrinsically involved in enabling learning that once‐relevant information is no longer valid. © 2014 The Authors. Hippocampus Published by Wiley Periodicals, Inc.     

Dyslexics are impaired on implicit higher-order sequence learning, but not on implicit spatial context learning

Developmental dyslexia is characterized by poor reading ability and impairments on a range of tasks including phonological processing and processing of sensory information. Some recent studies have found deficits in implicit sequence learning using the serial reaction time task, but others have not. Other skills, such as global visuo-spatial processing may even be enhanced in dyslexics, although deficits have also been noted. The present study compared dyslexic and non-dyslexic college students on two implicit learning tasks, an alternating serial response time task in which sequential dependencies exist across non-adjacent elements and a spatial context learning task in which the global configuration of a display cues the location of a search target. Previous evidence indicates that these implicit learning tasks are based on different underlying brain systems, fronto-striatal-cerebellar circuits for sequence learning and medial temporal lobe for spatial context learning. Results revealed a double dissociation: dyslexics showed impaired sequence learning, but superior spatial context learning. Consistent with this group difference, there was a significant positive correlation between reading ability (single real and non-word reading) and sequence learning, but a significant negative correlation between these measures and spatial context learning. Tests of explicit knowledge confirmed that learning was implicit for both groups on both tasks. These findings indicate that dyslexic college students are impaired on some kinds of implicit learning, but not on others. The specific nature of their learning deficit is consistent with reports of physiological and anatomical differences for individuals with dyslexia in frontal and cerebellar structures.     

The effect of electroconvulsive therapy (ECT) on implicit memory: skill learning and perceptual priming in patients with major depression

While explicit memory in amnesics is impaired, their implicit memory remains preserved. Memory impairment is one of the side effects of electroconvulsive therapy (ECT). ECT patients are expected to show impairment on explicit but not implicit tasks. The present study examined 17 normal controls and 17 patients with severe major depressive disorder who underwent right unilateral ECT. Patients were tested in three sessions: 24-48 hours prior to, 24-48 hours following the first ECT, and 24-48 hours following the eighth ECT. The controls were tested in three sessions, at time intervals that paralleled those of the patients. Implicit memory was tested by the perceptual priming task - Partial Picture-Identification (PPI). The skill learning task used entailed solving the Tower of Hanoi puzzle (TOHP). Explicit memory was tested by picture recall from the PPI task, verbal recall of information regarding the TOHP, and by the Visual Paired Association (VPA) test. Results showed that explicit questions about the implicit tasks were impaired following ECT treatment. Patients' learning ability, as measured by the VPA task, was only impaired in the first testing session, prior to ECT treatment, reflecting the effect of depression. In addition, groups only differed in the first session on the learning rate of the skill learning task. Perceptual priming was preserved in the patients' group in all sessions, indicating that it is resilient to the effect of depression and ECT. The results are interpreted in terms of the differential effect of depression and ECT on explicit and implicit memory.     

Face–name association learning in early Alzheimer's disease: A comparison of learning methods and their underlying mechanisms

This study compared the efficacy of five learning methods in the acquisition of face–name associations in early dementia of Alzheimer type (AD). The contribution of error production and implicit memory to the efficacy of each method was also examined. Fifteen participants with early AD and 15 matched controls were exposed to five learning methods: spaced retrieval, vanishing cues, errorless, and two trial-and-error methods, one with explicit and one with implicit memory task instructions. Under each method, participants had to learn a list of five face–name associations, followed by free recall, cued recall and recognition. Delayed recall was also assessed. For AD, results showed that all methods were efficient but there were no significant differences between them. The number of errors produced during the learning phases varied between the five methods but did not influence learning. There were no significant differences between implicit and explicit memory task instructions on test performances. For the control group, there were no differences between the five methods. Finally, no significant correlations were found between the performance of the AD participants in free recall and their cognitive profile, but generally, the best performers had better remaining episodic memory. Also, case study analyses showed that spaced retrieval was the method for which the greatest number of participants (four) obtained results as good as the controls. This study suggests that the five methods are effective for new learning of face–name associations in AD. It appears that early AD patients can learn, even in the context of error production and explicit memory conditions.