Declarative and nondeclarative sequence learning tasks: closed-head injured patients versus control participants

Patients who sustained closed-head injury (CHI) have been shown to have impaired memory for temporal order when measured under intentional, but not incidental, retrieval conditions. A group of 26 patients who sustained CHI and a matched control group of 26 individuals were tested on a declarative sequence learning task--"Chain Making" (CM), and a nondeclarative sequence learning task--Tower of Hanoi puzzle (TOHP). The TOHP is a problem solving task that requires planning and a strategic approach. The latter are cognitive processes known to be impaired following frontal lobe damage, as has been frequently documented in CHI patients. The goal of the present study was to test whether CHI patients' nondeclarative learning as measured by the TOHP task is preserved, as seen in amnesic patients, or impaired, as would be predicted following frontal lobe damage. Half of the participants in each group underwent active training, and the other half went through passive training of the tasks. The results demonstrate that the control group outperformed the CHI group (in most measures) in both declarative and nondeclarative sequence learning tasks. The effect of type of training differed for the two tasks: while performance of the control group on the TOHP was better under passive training (CHI patients did not improve on either one of the training modes), performance on the CM task was better under active training for both groups. The results are discussed in light of the role of the frontal lobes in memory generally, and in sequence learning particularly.     

Declarative and Nondeclarative Sequence Learning Tasks: Closed-Head Injured Patients Versus Control Participants

Patients who sustained closed-head injury (CHI) have been shown to have impaired memory for temporal order when measured under intentional, but not incidental, retrieval conditions. A group of 26 patients who sustained CHI and a matched control group of 26 individuals were tested on a declarative sequence learning task - Chain Making (CM), and a nondeclarative sequence learning - Tower of Hanoi puzzle (TOHP). The TOHP is a problem solving task that requires planning and a strategic approach. The latter are cognitive processes known to be impaired following frontal lobe damage, as has been frequently documented in CHI patients. The goal of the present study was to test whether CHI patients nondeclarative learning as measured by the TOHP task is preserved, as seen in amnesic patients, or impaired, as would be predicted following frontal lobe damage. Half of the participants in each group underwent active training, and the other half went through passive training of the tasks. The results demonstrate that the control group outperformed the CHI group (in most measures) in both declarative and nondeclarative sequence learning tasks. The effect of type of training differed for the two tasks: while performance of the control group on the TOHP was better under passive training (CHI patients did not improve on either one of the training modes), performance on the CM task was better under active training for both groups. The results are discussed in light of the role of the frontal lobes in memory generally, and in sequence learning particularly.     

Do children with developmental dyslexia have an implicit learning deficit?

OBJECTIVE: The purpose of this study was to investigate the effects of specific types of tasks on the efficiency of implicit procedural learning in the presence of developmental dyslexia (DD). METHODS: Sixteen children with DD (mean (SD) age 11.6 (1.4) years) and 16 matched normal reader controls (mean age 11.4 (1.9) years) were administered two tests (the Serial Reaction Time test and the Mirror Drawing test) in which implicit knowledge was gradually acquired across multiple trials. Although both tests analyse implicit learning abilities, they tap different competencies. The Serial Reaction Time test requires the development of sequential learning and little (if any) procedural learning, whereas the Mirror Drawing test involves fast and repetitive processing of visuospatial stimuli but no acquisition of sequences. RESULTS: The children with DD were impaired on both implicit learning tasks, suggesting that the learning deficit observed in dyslexia does not depend on the material to be learned (with or without motor sequence of response action) but on the implicit nature of the learning that characterises the tasks. CONCLUSION: Individuals with DD have impaired implicit procedural learning.     

NMDA receptor activity in learning spatial procedural strategies: I. The influence of hippocampal lesions

To acquire knowledge about the environment two types of learning are necessary: declarative localizatory learning about where environmental cues and the subject are, and procedural learning about how to explore and move around the environment. Experimental data indicate that hippocampal regions are involved in spatial learning, playing a key role in building spatial cognitive maps. The contribution of hippocampal NMDA receptors to spatial functions is indicated by the disruption of place learning when NMDA long-term potentiation is blocked. Conversely, the hippocampal contribution to the acquisition of procedural strategies is still controversial. Inactivation of the hippocampus by antagonizing the activity of AMPA/kainate receptors results in impaired spatial procedural learning. However, in the presence of a blockade of NMDA long-term potentiation in hippocampal areas it is still possible to learn explorative strategies. To investigate the involvement of the hippocampal NMDA receptors in spatial procedural learning, an NMDA receptor antagonist (CGS 19755) was administered i.p. to unlesioned animals or to animals with total ablation of hippocampal structures that had been tested in the Morris water maze. The CGS administration induced peripheral circling in both unlesioned control animals and in rats with bilateral hippocampal ablation. Conversely, circling was not observed if the drug-treated animals (either unlesioned or lesioned) had been spatially trained before drug administration. These findings indicate that even in the absence of the hippocampal formation the NMDA receptor antagonist found a site of action to influence the acquisition of spatial procedures to search for the platform.     

NMDA receptor activity in learning spatial procedural strategies I. The influence of hippocampal lesions

To acquire knowledge about the environment two types of learning are necessary: declarative localizatory learning about where environmental cues and the subject are, and procedural learning about how to explore and move around the environment. Experimental data indicate that hippocampal regions are involved in spatial learning, playing a key role in building spatial cognitive maps. The contribution of hippocampal NMDA receptors to spatial functions is indicated by the disruption of place learning when NMDA long-term potentiation is blocked. Conversely, the hippocampal contribution to the acquisition of procedural strategies is still controversial. Inactivation of the hippocampus by antagonizing the activity of AMPA/kainate receptors results in impaired spatial procedural learning. However, in the presence of a blockade of NMDA long-term potentiation in hippocampal areas it is still possible to learn explorative strategies. To investigate the involvement of the hippocampal NMDA receptors in spatial procedural learning, an NMDA receptor antagonist (CGS 19755) was administered i.p. to unlesioned animals or to animals with total ablation of hippocampal structures that had been tested in the Morris water maze. The CGS administration induced peripheral circling in both unlesioned control animals and in rats with bilateral hippocampal ablation. Conversely, circling was not observed if the drug-treated animals (either unlesioned or lesioned) had been spatially trained before drug administration. These findings indicate that even in the absence of the hippocampal formation the NMDA receptor antagonist found a site of action to influence the acquisition of spatial procedures to search for the platform.     

Dissociation between the procedural learning of letter names and motor sequences in developmental dyslexia

Motor sequence learning has been studied extensively in Developmental dyslexia (DD). The purpose of the present research was to examine procedural learning of letter names and motor sequences in individuals with DD and control groups. Both groups completed the Serial Search Task which enabled the assessment of learning of letter names and motor sequences independently of each other. Control participants learned both the letter names as well as the motor sequence. In contrast, individuals with DD were impaired in learning of the letter names sequence and showed a reliable transfer of the motor sequence. Previous studies proved that motor sequence learning is impaired in DD. The present study demonstrated that this deficit is more pronounced when the task to be learned involves linguistic units. This result implies that the procedural learning system of language is more deficient than the motor procedural learning system in individuals with DD. The dissociation between motor and letter names sequence learning in those with DD also implies that the systems underlying these two tasks are separable.     

Recognition memory for single items and for associations in amnesic patients

Recognition memory performance reflects two distinct processes or types of memory referred to as recollection and familiarity. According to theoretical claims about the two types of memory, single item and associative recognition tasks can be used as an experimental method to distinguish recollection and familiarity processes. Associative recognition decisions can be used as an index of recollection while memory for single items is mostly based on familiarity judgement. We employed this procedure to examine a possible dissociation in the memory performance of amnesic patients between spared single item and impaired associative recognition. Twelve amnesic patients, six with damage confined to the hippocampus proper, and six with damage elsewhere in the brain, were recruited for the present study. The findings showed that hippocampal amnesics exhibit relative sparing of single item learning but are consistently deficient in the learning of all kinds of between-item associations. These results are consistent with the view that hippocampal formation contributes differently to declarative tasks that require recollective or familiarity processes.     

Slow information processing after very severe closed head injury: impaired access to declarative knowledge and intact application and acquisition of procedural knowledge

As an explanation of the pattern of slow information processing after closed head injury (CHI), hypotheses of impaired access to declarative memory and intact application and acquisition of procedural memory after CHI are presented. These two hypotheses were tested by means of four cognitive reaction-time tasks, a semantic memory task, a memory comparison task, a mental rotation task and a mirror reading task. These tasks were administered on two different days to 12 survivors of a CHI tested more than 5 years after injury and a healthy control group of comparable age and education. In three tasks the difficulty of access to declarative knowledge was varied and it was expected that this would slow the CHI group more than the controls. In two tasks opportunities for procedural learning were provided by repeatedly presenting the same cognitive tasks and in one task, the difficulty of access to procedural memory was varied. It was expected that the CHI group would profit as much from this as would the control group. Both hypotheses were supported.     

Functional dissociation between fornix and hippocampus in spatial conditional learning

Do lesions of the fornix or the hippocampus impair the performance of spatial conditional associative learning tasks, and to what extent does damage to these brain structures result in comparable deficits in this type of spatial behavior? The available evidence is not clear. In the present study, rats with lesions of the fornix, hippocampus, and normal control animals were trained on two spatial–visual conditional learning tasks in which they had to form arbitrary associations between visual stimuli and the context in which these stimuli were embedded. In one condition, rats were required to choose stimulus X in place A and stimulus Y in place B, and there was no overlap in the contents of the two scenes. In the other condition, the animal approached the same scene from two different directions and had to select stimulus X when the scene was viewed from perspective A and to select stimulus Y when the scene was viewed from perspective B. Rats with fornix transection were able to learn both conditional tasks at a rate comparable to that of normal control animals, but rats with hippocampal damage were severely impaired under both conditions. The findings extend the range of tasks known to be sensitive to damage of the hippocampus. In addition, the results argue that the fornix is not necessary for the acquisition of certain spatial conditional learning tasks and that this brain structure cannot be used as an indicator of hippocampal dysfunction under all learning situations. © 2007 Wiley‐Liss, Inc.     

Evidence for parallel explicit and implicit sequence learning systems in older adults

Some research indicates that explicit learning of a sequence can impair procedural learning, particularly in populations with reduced cognitive capacity. However, these studies usually do not distinguish the effects of explicit processes on procedural learning from their effects on performance. The current study demonstrates that explicit learning affects performance, but not procedural sequence learning, in healthy older adults even when sequences are complex. These findings support capacity-independent theories which propose that procedural and declarative learning operate in parallel.     

Procedural memory during posttraumatic amnesia in survivors of severe closed head injury. Implications for rehabilitation

To investigate the possibility that learning of skills (ie, procedural memory) is preserved during posttraumatic amnesia, 16 amnesic survivors of severe closed head injury and 16 control subjects were studied. Procedural learning tasks included mirror reading, mazes, and a pursuit rotor task that involved tracking a rotating target. Declarative memory was assessed by testing recognition of the words used in mirror reading and a questionnaire concerning details of the previous testing session. Learning was evaluated on 3 consecutive days and a fourth session was scheduled after resolution of posttraumatic amnesia. Despite stable impairment of declarative memory during posttraumatic amnesia, the performance of head-injured patients improved across sessions on all procedural tasks and showed transfer to testing after resolution of posttraumatic amnesia.     

Procedural learning is impaired in dyslexia: Evidence from a meta-analysis of serial reaction time studies

A number of studies have investigated procedural learning in dyslexia using serial reaction time (SRT) tasks. Overall, the results have been mixed, with evidence of both impaired and intact learning reported. We undertook a systematic search of studies that examined procedural learning using SRT tasks, and synthesized the data using meta-analysis. A total of 14 studies were identified, representing data from 314 individuals with dyslexia and 317 typically developing control participants. The results indicate that, on average, individuals with dyslexia have worse procedural learning abilities than controls, as indexed by sequence learning on the SRT task. The average weighted standardized mean difference (the effect size) was found to be 0.449 (CI₉₅: .204, .693), and was significant (p < .001). However, moderate levels of heterogeneity were found between study-level effect sizes. Meta-regression analyses indicated that studies with older participants that used SRT tasks with second order conditional sequences, or with older participants that used sequences that were presented a large number of times, were associated with smaller effect sizes. These associations are discussed with respect to compensatory and delayed memory systems in dyslexia.     

Item Priming and Skill Learning in Amnesia

Abstract

This study employed a semantic decision-making task to examine both item priming and skill learning in amnesia, which traditionally have been demonstrated with separate tasks. Fourteen amnesic patients of mixed etiologies and 14 normal control subjects judged whether words represented animate or inanimate objects. One list was presented repeatedly on four continuous blocks of trials, and a new list was presented on the fifth block. For both groups, decision times decreased significantly from Block 1 to Block 5 (indicating skill acquisition) and increased significantly from Block 4 to Block 5 (indicating item-specific learning). The amnesic patients demonstrated a normal rate of skill learning, but a reduced magnitude of item priming. As expected, the amnesics had significantly impaired explicit memory of the implicitly learned items, as measured by recognition accuracy. The results suggest that both implicit and explicit learning of individual items is impaired in amnesia, despite normal semantic skill learning.     

Not so fast: Hippocampal amnesia slows word learning despite successful fast mapping

The human hippocampus is widely believed to be necessary for the rapid acquisition of new declarative relational memories. However, processes supporting on‐line inferential word use (“fast mapping”) may also exercise a dissociable learning mechanism and permit rapid word learning without the hippocampus (Sharon et al. (2011) Proc Natl Acad Sci USA 108:1146–1151). We investigated fast mapping in severely amnesic patients with hippocampal damage (N = 4), mildly amnesic patients (N = 6), and healthy comparison participants (N = 10) using on‐line measures (eye movements) that reflected ongoing processing. All participants studied unique word‐picture associations in two encoding conditions. In the explicit‐encoding condition, uncommon items were paired with their names (e.g., “This is a numbat.”). In the fast mapping study condition, participants heard an instruction using a novel word (e.g., “Click on the numbat.”) while two items were presented (an uncommon target such as a numbat, and a common distracter such as a dog). All groups performed fast mapping well at study, and on‐line eye movement measures did not reveal group differences. However, while comparison participants showed robust word learning irrespective of encoding condition, severely amnesic patients showed no evidence of learning after fast mapping or explicit encoding on any behavioral or eye‐movement measure. Mildly amnesic patients showed some learning, but performance was unaffected by encoding condition. The findings are consistent with the following propositions: the hippocampus is not essential for on‐line fast mapping of novel words; but is necessary for the rapid learning of arbitrary relational information irrespective of encoding conditions. © 2014 Wiley Periodicals, Inc.     

Spatial conditional associative learning: effects of thalamo-hippocampal disconnection in rats

Unilateral lesions to the anterior thalamic nuclei (ATN) and the hippocampus (H) were made in opposite hemispheres in the rat to examine whether these brain structures form part of a functional neural pathway underlying spatial learning and memory. In the first experiment, rats were tested on a spatial-visual conditional associative task in which they had to learn to approach one of two stimuli depending on the spatial context in which the stimuli were embedded. The rats were subsequently trained on delayed forced alternation, a spatial working memory task known to be sensitive to the effects of ATNxH damage. Rats with ATNxH lesions were impaired in the acquisition of both tasks in comparison with normal control animals. The findings support the idea that the anterior thalamic nuclei and the hippocampus are critical components of an anatomical system subserving spatial memory and suggest that these brain regions work in a dependent fashion during the performance of certain spatial learning tasks.     

Explicit and implicit remembering: when is learning preserved in amnesia?

Amnesic patients can learn and retain a variety of skills. To investigate what distinguishes tasks that are within the learning abilities of amnesic patients from those that are not, we administered two tests to individuals with Korsakoff's syndrome and two control groups. One was a visual reaction time task with an embedded repeating sequence of stimulus positions. Response times of Korsakoff patients indicated that they learned this sequence and retained it normally for a week. The second task was a tactual stylus maze in which all blind alleys were blocked. Korsakoff patients were impaired in learning this maze, as assessed by the time required to trace it. Differences between the two tasks are outlined and the implications of these differences are discussed.     

Hand gestures support word learning in patients with hippocampal amnesia

Co‐speech hand gesture facilitates learning and memory, yet the cognitive and neural mechanisms supporting this remain unclear. One possibility is that motor information in gesture may engage procedural memory representations. Alternatively, iconic information from gesture may contribute to declarative memory representations mediated by the hippocampus. To investigate these alternatives, we examined gesture's effects on word learning in patients with hippocampal damage and declarative memory impairment, with intact procedural memory, and in healthy and in brain‐damaged comparison groups. Participants learned novel label‐object pairings while producing gesture, observing gesture, or observing without gesture. After a delay, recall and object identification were assessed. Unsurprisingly, amnesic patients were unable to recall the labels at test. However, they correctly identified objects at above chance levels, but only if they produced a gesture at encoding. Comparison groups performed well above chance at both recall and object identification regardless of gesture. These findings suggest that gesture production may support word learning by engaging nondeclarative (procedural) memory.     

Ibotenate Lesions of Hippocampus and/or Subiculum: Dissociating Components of Allocentric Spatial Learning

This study examined the effects of ibotenic acid-induced lesions of the hippocampus, subiculum and hippocampus +/- subiculum upon the capacity of rats to learn and perform a series of allocentric spatial learning tasks in an open-field water maze. The lesions were made by infusing small volumes of the neurotoxin at a total of 26 (hippocampus) or 20 (subiculum) sites intended to achieve complete target cell loss but minimal extratarget damage. The regional extent and axon-sparing nature of these lesions was evaluated using both cresyl violet and Fink - Heimer stained sections. The behavioural findings indicated that both the hippocampus and subiculum lesions caused impairment to the initial postoperative acquisition of place navigation but did not prevent eventual learning to levels of performance almost as effective as those of controls. However, overtraining of the hippocampus + subiculum lesioned rats did not result in significant place learning. Qualitative observations of the paths taken to find a hidden escape platform indicated that different strategies were deployed by hippocampal and subiculum lesioned groups. Subsequent training on a delayed matching to place task revealed a deficit in all lesioned groups across a range of sample choice intervals, but the subiculum lesioned group was less impaired than the group with the hippocampal lesion. Finally, unoperated control rats given both the initial training and overtraining were later given either a hippocampal lesion or sham surgery. The hippocampal lesioned rats were impaired during a subsequent retention/relearning phase. Together, these findings suggest that total hippocampal cell loss may cause a dual deficit: a slower rate of place learning and a separate navigational impairment. The prospect of unravelling dissociable components of allocentric spatial learning is discussed.     

Cerebellar contribution to spatial event processing: do spatial procedures contribute to formation of spatial declarative knowledge?

Spatial knowledge of an environment involves two distinct competencies: declarative spatial knowledge, linked to where environmental cues are and where the subject is with respect to the cues, and, at the same time, procedural spatial knowledge, linked to how to move into the environment. It has been previously demonstrated that hemicerebellectomized (HCbed) rats are impaired in developing efficient exploration strategies, but not in building spatial maps or in utilizing localizing cues. The aim of the present study was to analyse the relationships between spatial procedural and declarative knowledge by using the open field test. HCbed rats have been tested in two different protocols of the open field task. The results indicate that HCbed animals succeeded in moving inside the arena, in contacting the objects and in habituating to the new environment. However, HCbed animals did not react to environmental changes, when their impaired explorative pattern was inappropriate to the environment, suggesting that they were not able to represent a new environment because they were not able to explore it appropriately. Nevertheless, when their altered procedures were favoured by object arrangement, they detected environmental changes as efficiently as did normal rats. This finding suggests that no declarative spatial learning is possible without appropriate procedural spatial learning.     

Procedural memory in Korsakoff's disease under different movement feedback conditions

Within the field of cognitive neuroscience, it has become widely accepted to distinguish between declarative and nondeclarative memory, with different neurobiological substrates subserving these memory structures. This distinction has been inferred from the study of amnesic patients, including those suffering from Korsakoff's syndrome. It is commonly agreed that Korsakoff patients demonstrate intact memory for motor and perceptual skills (nondeclarative) whereas memory of various forms of factual knowledge (declarative) is severely impaired. In the present study, Korsakoff patients and a group of age-matched controls learned a new bimanual motor skill whereby performance was assessed in the presence and absence of augmented visual information feedback. Findings demonstrated that Korsakoff patients were able to learn and retain this skill when directive augmented information feedback was provided while no learning occurred at all in the absence of this information. These observations shed new light on the conditions required for preserved memory in amnesic patients and challenge the classic view that nondeclarative memory is invariably preserved. Instead, the quality of memory across both motor and cognitive dimensions appears to depend on the availability of task-specific information to guide performance, presumably allowing amnesic patients to bypass affected brain areas. This prompts for a reevaluation of current notions about procedural memory capacity in Korsakoff patients.