An fMRI meta-analysis of the role of the striatum in everyday-life vs laboratory-developed habits

Guida, Pasqualina; Michiels, Mario; Redgrave, Peter; Luque, David; Obeso, Ignacio

doi:10.1101/2021.07.02.450904

Cited by 5 publications

(3 citation statements)

References 229 publications

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“…One potential mechanism could be an increase in inhibitory control over habit-driven behavior. This interpretation is consistent with findings that this region of the striatum has frequently been implicated in inhibitory control as well as habit learning and execution [69][70][71][72]. For example, a recent metaanalysis found that neural representations of both laboratory-produced habits and naturalistic habits acquired outside the laboratory are localized in the caudal putamen [70].…”

Section: Discussionsupporting

confidence: 88%

“…This interpretation is consistent with findings that this region of the striatum has frequently been implicated in inhibitory control as well as habit learning and execution[69-72]. For example, a recent meta-analysis found that neural representations of both laboratory-produced habits and naturalistic habits acquired outside the laboratory are localized in the caudal putamen[70]. Misconfiguration of this component of the habit execution circuit during acute abstinence may serve to reduce the propensity for habit-driven smoking behavior despite negative withdrawal symptoms.…”

Section: Discussionsupporting

confidence: 88%

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Dissociable misconfigurations of striatal functional connectivity profiles in smokers

Korponay

Stein²,

Ross³

2022

Preprint

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Corticostriatal circuits are central to reward processing and reinforcement learning functions that often become dysregulated in substance use disorder (SUD) and drive compulsive drug use. Human neuroimaging research seeking to identify how corticostriatal circuits become altered in SUD has primarily focused on evaluating connectivity between cortex-striatum node-pairs. Yet, striatal nodes receive appreciable input from many cortical nodes, and the morphological and electrophysiological properties of striatal nodes dictate that combinational features of their multivariate "connectivity profiles" shape their activity more so than any individual cortical node. Here, we introduce an approach for quantifying and statistically evaluating different types of multivariate connectivity profile configuration differences (i.e., aggregate divergence, rank order arrangement, and entropy shift) that may reflect different forms of circuit plasticity, and apply it to nicotine dependent smokers (n=46) as an exemplar SUD. Foremost, we find evidence of significant connectivity profile misconfiguration throughout much of the striatum, suggesting that prior findings of abnormal connections between individual striatal-cortical node-pairs may only represent the "tip of the iceberg" of corticostriatal circuit alteration in nicotine dependence. Moreover, we find that dorsolateral and ventromedial striatum display distinct types of connectivity profile misconfiguration. Whereas dorsolateral striatum almost exclusively displays abnormal rank order arrangement that is present in both the nicotine sated and acutely abstinent states - indicative of a "trait" misconfiguration - ventromedial striatum almost exclusively displays abnormal aggregate divergence that only manifests during acute abstinence - indicative of a "state" misconfiguration. Further, we identify a unique striatal site in the right caudal ventral putamen that displays multiple forms of connectivity profile misconfiguration, where connections with cognitive processing cortical areas overtake those with motor/premotor control cortical areas as the strongest in the connectivity profile, and acute abstinence significantly strengthens this abnormal arrangement. Moreover, the interactive magnitude of these misconfigurations during acute abstinence is significantly linked to dependence severity. Collectively, the present findings underscore the need for increased examination of connectivity profile misconfigurations as a mechanism of SUD etiology and as a potential guide for identifying therapeutic intervention targets.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionsupporting

confidence: 88%

Dissociable misconfigurations of striatal functional connectivity profiles in smokers

Korponay

Stein²,

Ross³

2022

Preprint

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“…Empirical validation that sequential tasks rely on habit learning comes from recent meta-analyses of neural activation studies (Guida et al, 2022;Patterson & Knowton, 2018). The habit-related sensorimotor network, especially the posterior dorsal putamen, supplementary motor area, and cerebellum, became activated when participants had extensively practiced motor-sequence-learning tasks.…”

Section: How Habits Guide Respondingmentioning

confidence: 99%

Measuring context–response associations that drive habits

Labrecque,

Lee,

Wood

2023

J Exper Analysis Behavior

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People achieve important life outcomes of health, financial security, and productivity by repeating operant behavior. To identify whether such operants reflect goal pursuit or habit, the present research introduces a new paradigm that yields objective measures of learning and controls for the motivations of goal pursuit. In two experiments, participants practiced a sequential task of making sushi and then completed a test of the strength of cue–response (habit) associations in memory. Finally, they repeated the sushi task without instructions while under cognitive load (designed to impede deliberation about goals). As predicted, greater task practice yielded stronger cue–response associations, which in turn promoted task success. Practice did not improve performance by enhancing goal intentions or other task motivations. We conclude that repetition facilitates performance by creating mental associations that automatically activate practiced, habitual responses upon perception of recurring context cues.

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Misconfigured striatal connectivity profiles in smokers

Korponay

Stein

Ross

2022

Neuropsychopharmacol.

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Dysregulation of frontal cortical inputs to the striatum is foundational in the neural basis of substance use disorder (SUD). Neuroanatomical and electrophysiological data increasingly show that striatal nodes receive appreciable input from numerous cortical areas, and that the combinational properties of these multivariate “connectivity profiles” play a predominant role in shaping striatal activity and function. Yet, how abnormal configuration of striatal connectivity profiles might contribute to SUD is unknown. Here, we implemented a novel “connectivity profile analysis” (CPA) approach using resting-state functional connectivity data to facilitate detection of different types of connectivity profile “misconfiguration” that may reflect distinct forms of aberrant circuit plasticity in SUD. We examined 46 nicotine-dependent smokers and 33 non-smokers and showed that both dorsal striatum (DS) and ventral striatum (VS) connectivity profiles with frontal cortex were misconfigured in smokers—but in doubly distinct fashions. DS misconfigurations were stable across sated and acute abstinent states (indicative of a “trait” circuit adaptation) whereas VS misconfigurations emerged only during acute abstinence (indicative of a “state” circuit adaptation). Moreover, DS misconfigurations involved abnormal connection strength rank order arrangement, whereas VS misconfigurations involved abnormal aggregate strength. We found that caudal ventral putamen in smokers uniquely displayed multiple types of connectivity profile misconfiguration, whose interactive magnitude was linked to dependence severity, and that VS misconfiguration magnitude correlated positively with withdrawal severity during acute abstinence. Findings underscore the potential for approaches that more aptly model the neurobiological composition of corticostriatal circuits to yield deeper insights into the neural basis of SUD.

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An fMRI meta-analysis of the role of the striatum in everyday-life vs laboratory-developed habits

Cited by 5 publications

References 229 publications

Dissociable misconfigurations of striatal functional connectivity profiles in smokers

Dissociable misconfigurations of striatal functional connectivity profiles in smokers

Measuring context–response associations that drive habits

Misconfigured striatal connectivity profiles in smokers

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