Dorsal striatum does not mediate feedback-based, stimulus-response learning: An event-related fMRI study in patients with Parkinson's disease tested on and off dopaminergic therapy

Nole M Hiebert; Adrian M Owen; Hooman Ganjavi; Daniel Mendonça; Mary E Jenkins; Ken N Seergobin; Penny A MacDonald

doi:10.1016/j.neuroimage.2018.10.045

Dorsal striatum does not mediate feedback-based, stimulus-response learning: An event-related fMRI study in patients with Parkinson's disease tested on and off dopaminergic therapy

Neuroimage. 2019 Jan 15:185:455-470. doi: 10.1016/j.neuroimage.2018.10.045. Epub 2018 Oct 27.

Authors

Nole M Hiebert¹, Adrian M Owen², Hooman Ganjavi³, Daniel Mendonça⁴, Mary E Jenkins⁴, Ken N Seergobin⁵, Penny A MacDonald⁶

Affiliations

¹ Brain and Mind Institute, University of Western Ontario, London, Ontario, N6A 5B7 Canada; Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, N6A 5C1, Canada.
² Brain and Mind Institute, University of Western Ontario, London, Ontario, N6A 5B7 Canada; Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, N6A 5C1, Canada; Department of Psychology, University of Western Ontario, London, Ontario, N6A 5C2, Canada.
³ Department of Psychiatry, University of Western Ontario, London, Ontario, N6C 0A7, Canada.
⁴ Department of Clinical Neurological Sciences, University of Western Ontario, London, Ontario, N6A 5A5, Canada.
⁵ Brain and Mind Institute, University of Western Ontario, London, Ontario, N6A 5B7 Canada; Department of Clinical Neurological Sciences, University of Western Ontario, London, Ontario, N6A 5A5, Canada.
⁶ Brain and Mind Institute, University of Western Ontario, London, Ontario, N6A 5B7 Canada; Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, N6A 5C1, Canada; Department of Psychology, University of Western Ontario, London, Ontario, N6A 5C2, Canada; Department of Clinical Neurological Sciences, University of Western Ontario, London, Ontario, N6A 5A5, Canada. Electronic address: penny.macdonald@lhsc.on.ca.

PMID: 30394326
DOI: 10.1016/j.neuroimage.2018.10.045

Abstract

Learning associations between stimuli and responses is essential to everyday life. Dorsal striatum (DS) has long been implicated in stimulus-response learning, though recent results challenge this contention. We have proposed that discrepant findings arise because stimulus-response learning methodology generally confounds learning and response selection processes. In 19 patients with Parkinson's disease (PD) and 18 age-matched controls, we found that dopaminergic therapy decreased the efficiency of stimulus-response learning, with corresponding attenuation of ventral striatum (VS) activation. In contrast, exogenous dopamine improved response selection accuracy related to enhanced DS BOLD signal. Contrasts between PD patients and controls fully support these within-subject patterns. These double dissociations in terms of behaviour and neural activity related to VS and DS in PD and in response to dopaminergic therapy, strongly refute the view that DS mediates stimulus-response learning through feedback. Our findings integrate with a growing literature favouring a role for DS in decision making rather than learning, and unite two literature that have been evolving independently.

Keywords: Decision making; Dopamine; Dorsal striatum; Functional magnetic resonance imaging; Ventral striatum.

Publication types

Randomized Controlled Trial
Research Support, Non-U.S. Gov't

MeSH terms

Aged
Antiparkinson Agents / therapeutic use
Association Learning / drug effects*
Association Learning / physiology*
Brain Mapping / methods
Corpus Striatum / drug effects*
Corpus Striatum / physiopathology
Decision Making / drug effects
Decision Making / physiology
Evoked Potentials / drug effects
Evoked Potentials / physiology
Female
Formative Feedback
Humans
Levodopa / therapeutic use*
Magnetic Resonance Imaging
Male
Parkinson Disease / drug therapy
Parkinson Disease / physiopathology
Parkinson Disease / psychology*

Substances

Antiparkinson Agents
Levodopa