Examining dorsal striatum in cognitive effort using Parkinson's disease and fMRI

MacDonald, Alex A.; Seergobin, Ken N.; Tamjeedi, Ruzbeh; Owen, Adrian M.; Provost, Jean-Sébastien; Monchi, Oury; Ganjavi, Hooman; MacDonald, Penny A.

doi:10.1002/acn3.62

Cited by 20 publications

(21 citation statements)

References 58 publications

(85 reference statements)

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“…We found that DS activity correlates only with decisions and response selections requiring deliberation but not with late‐stage, stimulus–response association learning. Our results challenge the notion that the DS underlies the development of automaticity, integrating rather with a growing literature suggesting that DS—particularly the caudate nucleus—mediates decision making [Cincotta and Seger, ; Little et al, ; Seger et al, ] when an element of deliberation is required [Atallah et al, ; Grahn et al, ; Hiebert et al, ; Jessup and O'Doherty, ; MacDonald et al, ; McDonald and Hong, ; Postle and D'Esposito, ; Smittenaar et al, ].…”

Section: Discussionsupporting

confidence: 67%

“…Indeed, a reinterpretation of these early‐ and late‐learning experiments, considering the facts that decision making and stimulus–response association learning (a) depend upon one another to produce accurate performance and (b) are often merged in fMRI studies, could integrate two divergent and extensive literatures regarding DS's role in cognition. Increasingly, DS is linked to response selection and decision making [Atallah et al, ; Grahn et al, ; Jessup and O'Doherty, ; MacDonald et al, ]. Decision making is defined as the process of representing and assigning values to different response possibilities, then selecting and executing the most appropriate action [Rangel et al, ].…”

Section: Introductionmentioning

confidence: 99%

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Dorsal striatum mediates deliberate decision making, not late‐stage, stimulus–response learning

Hiebert

Owen

Seergobin

et al. 2017

Human Brain Mapping

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We investigated a controversy regarding the role of the dorsal striatum (DS) in deliberate decision-making versus late-stage, stimulus-response learning to the point of automatization. Participants learned to associate abstract images with right or left button presses explicitly before strengthening these associations through stimulus-response trials with (i.e., Session 1) and without (i.e., Session 2) feedback. In Session 1, trials were divided into response-selection and feedback events to separately assess decision versus learning processes. Session 3 evaluated stimulus-response automaticity using a location Stroop task. DS activity correlated with response-selection and not feedback events in Phase 1 (i.e., Blocks 1-3), Session 1. Longer response times (RTs), lower accuracy, and greater intertrial variability characterized Phase 1, suggesting deliberation. DS activity extinguished in Phase 2 (i.e., Blocks 4-12), Session 1, once RTs, response variability, and accuracy stabilized, though stimulus-response automatization continued. This was signaled by persisting improvements in RT and accuracy into Session 2. Distraction between Sessions 1 and 2 briefly reintroduced response uncertainty, and correspondingly, significant DS activity reappeared in Block 1 of Session 2 only. Once stimulus-response associations were again refamiliarized and deliberation unnecessary, DS activation disappeared for Blocks 2-8, Session 2. Interference from previously learned right or left button responses with incongruent location judgments in a location Stroop task provided evidence that automaticity of stimulus-specific button-press responses had developed by the end of Session 2. These results suggest that DS mediates decision making and not late-stage learning, reconciling two, independently evolving and well-supported literatures that implicate DS in different cognitive functions. Hum Brain Mapp 38:6133-6156, 2017. © 2017 Wiley Periodicals, Inc.

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Section: Discussionsupporting

confidence: 67%

Section: Introductionmentioning

confidence: 99%

Dorsal striatum mediates deliberate decision making, not late‐stage, stimulus–response learning

Hiebert

Owen

Seergobin

et al. 2017

Human Brain Mapping

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“…Despite this, for all participants, no significant interference occurred in Session 3 when stimuli occurred in the location opposite to the spoken “right” or “left” response paired with them in Session 1. Dissociations between facilitation and interference effects in similar paradigms are commonly noted 11,28,30…”

Section: Discussionmentioning

confidence: 94%

Dopaminergic therapy affects learning and impulsivity in Parkinson's disease

Hiebert

Seergobin

et al. 2014

Ann Clin Transl Neurol

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ObjectiveThe aim was to examine the effect of dopaminergic medication on stimulus-response learning versus performing decisions based on learning.MethodTo see the effect of dopaminergic therapy on stimulus-response learning and response selection, participants with Parkinson’s disease (PD) were either tested on and/or off their prescribed dose of dopaminergic therapy during different testing days. Forty participants with PD and 34 healthy controls completed the experiment on consecutive days. On Day 1, participants learned to associate abstract images with spoken, “right” or “left” responses via feedback (Session 1). On Day 2, participants recalled these responses (Session 2) and indicated the location (i.e., right or left of center) of previously studied images intermixed with new images (Session 3).ResultsParticipants with PD off medication learned stimulus-response associations equally well compared to healthy controls. Learning was impaired by dopaminergic medication. Regardless of medication status, patients recalled the stimulus-response associations from Day 1 as well as controls. In Session 3 off medication, patients demonstrated enhanced facilitation relative to controls and patients on medication, when the stimulus location was congruent with the spoken response that was learned for the stimulus in Session 1.InterpretationLearning in PD was comparable to that of healthy controls off medication. Learning was worsened by dopaminergic therapy in PD. We interpret greater facilitation in participants with PD off medication for congruent responses as evidence of greater impulsivity. This motor or reflexive impulsivity was normalized by medication in PD. These findings shed light on the cognitive profile of PD and have implications for dopaminergic treatment.

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“…Classically, the putamen has primarily been considered a motor structure, and abnormal putamen structure and function are closely related to PD . MacDonald et al reported that the dorsal striatum (bulk of the caudate nucleus and the putamen) mediates cognitive flexibility and cognitive effort in PD . The lesser functional connectivity between MrD and putamen demonstrated the network impairment, and supports the hypothesis that MrD contributes to cognitive dysfunction in patients with PD.…”

Section: Discussionmentioning

confidence: 81%

Altered functional connectivity of the marginal division in Parkinson's disease with mild cognitive impairment: A pilot resting‐state fMRI study

Chen

et al. 2019

Magnetic Resonance Imaging

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Background The marginal division (MrD) is an important subcortical center involved in learning and memory. Mild cognitive impairment (MCI) is commonly seen in patients with Parkinson's disease (PD), but the neurobiological basis is yet to be elucidated. Purpose To use resting‐state functional magnetic resonance imaging (rs‐fMRI) to explore the altered functional connectivity (FC) of the MrD in patients with PD‐MCI. Study Type Prospective pilot study. Population Twenty‐five patients with PD‐MCI; 25 PD patients and no cognitive impairment (PD‐NCI); and 25 healthy control (HC) participants. Sequence 3.0 T GE Healthcare MRI scanner; three‐dimensional T1‐weighted fast spoiled gradient recalled echo (3D T1‐FSPGR); rs‐fMRI. Assessment The MrD was defined using manual delineation, which was the seed point to compute the FC to examine correlations between low‐frequency fMRI signal fluctuations in MrD and the whole brain. Statistical Tests Between‐group comparisons of the rs‐fMRI data were computed using two‐sample t‐tests in a voxelwise manner after controlling for age and sex, to determine the brain regions that showed significant differences in FC with the bilateral MrDs. Correlation analyses were performed for FC values and cognitive abilities in patients with PD. Results In the PD‐MCI group, compared with the PD‐NCI group, we observed lesser FC between the MrD bilaterally and right putamen, left insula, left cerebellum, and left thalamus; greater FC between the MrD bilaterally and left middle cingulate cortex, left middle frontal gyrus, left superior frontal gyrus, left supplementary motor area, and left middle/inferior occipital gyrus. Moreover, the strength of FC between the MrD and regions that showed differences between the PD‐MCI and PD‐NCI groups was significantly correlated with neuropsychological scores in patients with PD. Data Conclusion The current study suggests that MrD dysfunction may contribute to MCI in PD. However, the mechanisms underlying this process require further investigation. Level of Evidence 1. Technical Efficacy Stage 2. J. Magn. Reson. Imaging 2019;50:183–192.

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Examining dorsal striatum in cognitive effort using Parkinson's disease and fMRI

Cited by 20 publications

References 58 publications

Dorsal striatum mediates deliberate decision making, not late‐stage, stimulus–response learning

Dorsal striatum mediates deliberate decision making, not late‐stage, stimulus–response learning

Dopaminergic therapy affects learning and impulsivity in Parkinson's disease

Altered functional connectivity of the marginal division in Parkinson's disease with mild cognitive impairment: A pilot resting‐state fMRI study

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