Is implicit sequence learning impaired in Parkinson's disease? A meta-analysis.

Siegert, Richard J.; Taylor, Kathryn D.; Weatherall, Mark; Abernethy, David

doi:10.1037/0894-4105.20.4.490

Cited by 156 publications

(137 citation statements)

References 29 publications

(28 reference statements)

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“…Siegert et al 2006), whereas other investigators have suggested that DA may not be involved in the processing of sequential learning (for discussions on these opposed findings, see Werheid et al 2003;Badgaiyan et al 2007;Vandenbossche et al 2009). Nevertheless, models which propose the involvement of DAergic basal ganglia processes in sequential behavior are widely accepted (Graybiel 1998;Da Cunha et al 2009;Schwarting 2009).…”

Section: Introductionmentioning

confidence: 98%

6-Hydroxydopamine Lesions in the Rat Neostriatum Impair Sequential Learning in a Serial Reaction Time Task

et al. 2009

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Sequential behavior has been intensively investigated in humans using so-called serial reaction time tasks(SRTT), in which visual stimuli are either presented in a random or sequential order. Typically, when the stimulus presentation follows a previously learned sequential order,reaction times are decreased compared to random stimulus presentation and become partly automated. A vast amount of SRTT findings indicates that sequential learning and performance seem to be mediated amongst others by the basal ganglia-especially the striatum-and the neurotransmitter dopamine therein. In this study we used an operant rat version of the human four choice SRTT to investigate the effect of bilateral neostriatal dopamine lesions induced by 6-hydroxydopamine on sequential learning. The rats' task was to respond rapidly to illuminated holes by nose-poking into them. During extensive training, the position of the illuminated hole followed a 12-item sequence. The outcome of this sequential training was also investigated in two tests, namely an interference test, where stimulus presentation switched between this sequential and a pseudo random order every five minutes, and a violation test, in which only one sequence item was eventually skipped. The neurotoxic lesions, which was placed before the start of training, led to the expected sub-total dopamine depletions (i.e. residual levels around 34-56% of controls), especially in the medial neostriatum. These lesions did not lead to general motor deficits in a catalepsy task, but moderate deficits in locomotion in an activity box, which largely recovered with time after lesion. In the SRTT, rats with lesions showed impaired learning, that is, less response accuracy and slower reaction times than the control group.During a subsequent test with alternating phases of sequential and random stimulus presentations, reaction times and accuracy of the control group were superior during sequential as compared to random stimulus phases. In the lesion group, only a moderate advantage in accuracy was observed. In the violation test, another outcome measure, the control group showed an expected increase in reaction times on the violated positions. By contrast, the lesion group showed no such increase, which indicates less automation of sequential behavior in these animals. For one, these findings support previous evidence in showing that neostriatal dopamine plays an important role for instrumental behavior, in general. Furthermore,and most importantly, they suggest that dopaminergic-striatal networks also play an important role in sequential behavior, especially its acquisition.

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Section: Introductionmentioning

confidence: 98%

6-Hydroxydopamine Lesions in the Rat Neostriatum Impair Sequential Learning in a Serial Reaction Time Task

et al. 2009

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“…On the basis of clinical SRTT studies in which Parkinson's disease patients showed deficits in sequential learning (for review see Siegert et al, 2006) and imaging studies revealing striatal recruitment during sequential learning (e.g., Werheid et al, 2003;Badgaiyan et al, 2007), various models were proposed that suggest a crucial role for dopaminergic processes in the striatum in sequential learning (Graybiel, 1998;Doyon and Ungerleider, 2002;Packard and Knowlton, 2002;Da Cunha et al, 2009;Schwarting, 2009). In a recent series of experiments using our rat version of the SRTT (Domenger and Schwarting 2005, 2007, we were able to lend further empirical support to the models' notion of the dependency of sequential learning on striatal dopamine availability Schwarting, 2008, Eckart et al, 2010a,b).…”

Section: Introductionmentioning

confidence: 99%

Dorsal hippocampal lesions boost performance in the rat sequential reaction time task

2011

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It is commonly accepted that the hippocampus plays a major role in declarative memory across species and that it is of particular relevance for spatial memory in rodents. However, the interplay between hippocampal function and nondeclarative memory systems, such as procedural stimulus-response (S-R) or sequential learning, is less clear: depending on task requirements, an interaction, dissociation or interference between hippocampal function and other memory systems may occur. This study was conducted to investigate the influence of dorsal ibotenic hippocampal lesions on learning and performance of sequential behavior in a rat version of the serial reaction time task (SRTT). Magnetic resonance imaging (MRI) analyses of the lesions revealed a bilateral volume reduction of ≈ 46% (histological analyses: ≈ 59%) of the total hippocampus. They were largely confined to its dorsal part and led to an expected spatial memory deficits in an object place recognition test as compared to healthy controls, even though sham lesions had the same effect. Our earlier studies on sequential learning had revealed substantial impairments in case of dorsal striatal dopaminergic lesions. In the present study, however, hippocampal lesioned animals unexpectedly showed superior performance throughout SRTT testing and training as compared to controls, which resulted in a higher degree of subsequent automated sequential behavior. Thus, our data reveal the infrequent case where hippocampal lesions lead to long-term improvements in test performance of a type of rather complex procedural behavior. One possible explanation for this effect is that hippocampal activity in rodents can interfere with other memory systems during the acquisition of procedural tasks with very low spatial requirements, as used here. Alternative explanations for the observed superior SRTT performance in lesioned animals, such as hyperactivity or increased exploratory drive are also topic of the discussion.

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“…Disease of these brain regions has been associated with impaired procedural memory. Individuals with Parkinson's disease are impaired on procedural memory tasks, such as probabilistic classification learning and motor sequence learning (Knowlton et al, 1996;Siegert, Taylor, Weatherall, & Abernethy, 2006;Wilkinson, Khan, & Jahanshahi, 2009). Conversely, a study with the famous amnesic individual, H. M., showed that while he had profound declarative memory impairment due to medial temporal lobe damage, he was able to learn how to use a stylus to perform a mirror tracing task.…”

Section: Procedural Memory and Toolsmentioning

confidence: 99%

Effects of dividing attention on memory for declarative and procedural aspects of tool use

Roy

Park

2016

Mem Cogn

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Tool-related knowledge and skills are supported by a complex set of memory processes that are not well understood. Some aspects of tools are mediated by either declarative or procedural memory, while other aspects may rely on an interaction of both systems. Although motor skill learning is believed to be primarily supported by procedural memory, there is debate in the current literature regarding the role of declarative memory. Growing evidence suggests that declarative memory may be involved during early stages of motor skill learning, although findings have been mixed. In the current experiment, healthy, younger adults were trained to use a set of novel complex tools and were tested on their memory for various aspects of the tools. Declarative memory encoding was interrupted by dividing attention during training. Findings showed that dividing attention during training was detrimental for subsequent memory for tool attributes as well as accurate demonstration of tool use and tool grasping. However, dividing attention did not interfere with motor skill learning, suggesting that declarative memory is not essential for skill learning associated with tools.

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Is implicit sequence learning impaired in Parkinson's disease? A meta-analysis.

Cited by 156 publications

References 29 publications

6-Hydroxydopamine Lesions in the Rat Neostriatum Impair Sequential Learning in a Serial Reaction Time Task

6-Hydroxydopamine Lesions in the Rat Neostriatum Impair Sequential Learning in a Serial Reaction Time Task

Dorsal hippocampal lesions boost performance in the rat sequential reaction time task

Effects of dividing attention on memory for declarative and procedural aspects of tool use

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