The role of the striatum in implicit learning: a functional magnetic resonance imaging study

Reiss, Jeffrey P.; Campbell, Darren W.; Leslie, William D.; Paulus, Martin P.; Stroman, Patrick W.; Polimeni, Joseph; Malcolmson, Kelly A; Sareen, Jitender

doi:10.1097/01.wnr.0000175615.93312.1a

Cited by 56 publications

(33 citation statements)

References 20 publications

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“…In order that external input (Robertson 2009) and internal interactions between different memory systems (Poldrack et al 2001;Brown and Robertson 2007) should not interfere with this process, it has been proposed that it takes place during sleep (Born et al 2006;Walker 2009). Our findings support and extend this, suggesting that this is the case not only for declarative tasks but also procedural tasks in which a transfer from the MTL to the striatum takes place over time (Reiss et al 2005;Rieckmann et al 2010).…”

Section: A C C E P T E D Accepted Manuscriptsupporting

confidence: 86%

Cross-modal transfer of statistical information benefits from sleep

Durrant

Cairney

Lewis

2016

Cortex

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Extracting regularities from a sequence of events is essential for understanding our environment. However, there is no consensus regarding the extent to which such regularities can be generalised beyond the modality of learning. One reason for this could be the variation in consolidation intervals used in different paradigms, also including an opportunity to sleep. Using a novel statistical learning paradigm in which structured information is acquired in the auditory domain and tested in the visual domain over either 30min or 24hr consolidation intervals, we show that cross-modal transfer can occur, but this transfer is only seen in the 24hr group. Importantly, the extent of cross-modal transfer is predicted by the amount of SWS obtained. Additionally, cross-modal transfer is associated with the same pattern of decreasing MTL and increasing striatal involvement which has previously been observed to occur across 24 hours in unimodal statistical learning. We also observed enhanced functional connectivity after 24 hours in a network of areas which have been implicated in cross-modal integration including the precuneus and the middle occipital gyrus. Finally, functional connectivity between the striatum and the precuneus was also enhanced, and this strengthening was predicted by SWS. These results demonstrate that statistical learning can generalise to some extent beyond the modality of acquisition, and together with our previously published unimodal results, support the notion that statistical learning is both domain-general and domain-specific.

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Section: A C C E P T E D Accepted Manuscriptsupporting

confidence: 86%

Cross-modal transfer of statistical information benefits from sleep

Durrant

Cairney

Lewis

2016

Cortex

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“…In functional neuroimaging studies, dorsal striatum is preferentially activated for learned relative to random motor sequences [91], for familiar items in an episodic recognition test [20], and while recalling recently-learned category membership [92], [93]. Unlike activity in ventral striatum that tracks the progression of learning, dropping off as performance asymptotes and hence learning plateaus [4], [91], [93], preferential activation of the dorsal striatum in neuroimaging studies persists well after sequences or categorization rules [93] have been encoded. Together these findings suggest that although dorsal striatum is implicated in explicit memory function, it does not underlie learning or encoding processes.…”

Section: Discussionmentioning

confidence: 99%

Differential Effects of Parkinson's Disease and Dopamine Replacement on Memory Encoding and Retrieval

et al. 2013

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Increasingly memory deficits are recognized in Parkinson's disease (PD). In PD, the dopamine-producing cells of the substantia nigra (SN) are significantly degenerated whereas those in the ventral tegmental area (VTA) are relatively spared. Dopamine-replacement medication improves cognitive processes that implicate the SN-innervated dorsal striatum but is thought to impair those that depend upon the VTA-supplied ventral striatum, limbic and prefrontal cortices. Our aim was to examine memory encoding and retrieval in PD and how they are affected by dopamine replacement. Twenty-nine PD patients performed the Rey Auditory Verbal Learning Test (RAVLT) and a non-verbal analogue, the Aggie Figures Learning Test (AFLT), both on and off dopaminergic medications. Twenty-seven, age-matched controls also performed these memory tests twice and their data were analyzed to correspond to the ON-OFF order of the PD patients to whom they were matched. We contrasted measures that emphasized with those that accentuated retrieval and investigated the effect of PD and dopamine-replacement on these processes separately. For PD patients relative to controls, encoding performance was normal in the off state and was impaired on dopaminergic medication. Retrieval was impaired off medication and improved by dopamine repletion. This pattern of findings suggests that VTA-innervated brain regions such as ventral striatum, limbic and prefrontal cortices are implicated in encoding, whereas the SN-supplied dorsal striatum mediates retrieval. Understanding this pattern of spared functions and deficits in PD, and the effect of dopamine replacement on these distinct memory processes, should prompt closer scrutiny of patients' cognitive complaints to inform titration of dopamine replacement dosages along with motor symptoms.

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“…These studies, however, have focused almost exclusively on attention and executive functions that are highly influenced to some extent by dopaminergic dysfunction (Lange et al, 1992). Most studies examining how dopaminergic transmission influences learning and memory in early PD have focused primarily on working memory, incremental learning, and reward based learning, with few investigations focusing on the role of dopamine in declarative memory (Cools et al, 2003; Cools, Stefanova, Barker, Robbins, & Owen, 2002; Costa et al, 2003; Cropley et al, 2008; Fera et al, 2007; Fournet et al, 2000; Gotham et al, 1986; Jahanshahi et al, 2010; Kelly et al, 2009; Lange et al, 1992; McClure, Laibson, Loewenstein, & Cohen, 2004; Nagano-Saito et al, 2008; Reiss et al, 2005; Sawamoto et al, 2008; Seo, Beigi, Jahanshahi, & Averbeck, 2010; Shohamy, Myers, Geghman, Sage, & Gluck, 2006). Nonetheless, there have been several investigations evaluating the role of dopamine in memory recall and retention.…”

Section: Discussionmentioning

confidence: 99%

Paradoxical Effect of Dopamine Medication on Cognition in Parkinson’s Disease: Relationship to Side of Motor Onset

Hanna-Pladdy

Pahwa

Lyons

2015

J Int Neuropsychol Soc

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Parkinson's disease (PD) is characterized by asymmetric motor symptom onset attributed to greater degeneration of dopamine neurons contralateral to the affected side. However, whether motor asymmetries predict cognitive profiles in PD, and to what extent dopamine influences cognition remains controversial. This study evaluated cognitive variability in PD by measuring differential response to dopamine replacement therapy (DRT) based on hemispheric asymmetries. The influence of DRT on cognition was evaluated in mild PD patients (n = 36) with left or right motor onset symptoms. All subjects were evaluated on neuropsychological measures on and off DRT and compared to controls (n = 42). PD patients were impaired in executive, memory and motor domains irrespective of side of motor onset, although patients with left hemisphere deficit displayed greater cognitive impairment. Patients with right hemisphere deficit responded to DRT with significant improvement in sensorimotor deficits, and with corresponding improvement in attention and verbal memory functions. Conversely, patients with greater left hemisphere dopamine deficiency did not improve in attentional functions and declined in verbal memory recall following DRT. These findings support the presence of extensive mild cognitive deficits in early PD not fully explained by dopamine depletion alone. The paradoxical effects of levodopa on verbal memory were predicted by extent of fine motor impairment and sensorimotor response to levodopa, which reflects extent of dopamine depletion. The findings are discussed with respect to factors influencing variable cognitive profiles in early PD, including hemispheric asymmetries and differential response to levodopa based on dopamine levels predicting amelioration or overdosing.

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The role of the striatum in implicit learning: a functional magnetic resonance imaging study

Cited by 56 publications

References 20 publications

Cross-modal transfer of statistical information benefits from sleep

Cross-modal transfer of statistical information benefits from sleep

Differential Effects of Parkinson's Disease and Dopamine Replacement on Memory Encoding and Retrieval

Paradoxical Effect of Dopamine Medication on Cognition in Parkinson’s Disease: Relationship to Side of Motor Onset

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