Mesocorticolimbic hemodynamic response in Parkinson's disease patients with compulsive behaviors

Mov Disord. 2017 Nov;32(11):1574-1583. doi: 10.1002/mds.27047. Epub 2017 Jun 19.

Abstract

Background: PD patients treated with dopamine therapy can develop maladaptive impulsive and compulsive behaviors, manifesting as repetitive participation in reward-driven activities. This behavioral phenotype implicates aberrant mesocorticolimbic network function, a concept supported by past literature. However, no study has investigated the acute hemodynamic response to dopamine agonists in this subpopulation.

Objectives: We tested the hypothesis that dopamine agonists differentially alter mesocortical and mesolimbic network activity in patients with impulsive-compulsive behaviors.

Methods: Dopamine agonist effects on neuronal metabolism were quantified using arterial-spin-labeling MRI measures of cerebral blood flow in the on-dopamine agonist and off-dopamine states. The within-subject design included 34 PD patients, 17 with active impulsive compulsive behavior symptoms, matched for age, sex, disease duration, and PD severity.

Results: Patients with impulsive-compulsive behaviors have a significant increase in ventral striatal cerebral blood flow in response to dopamine agonists. Across all patients, ventral striatal cerebral blood flow on-dopamine agonist is significantly correlated with impulsive-compulsive behavior severity (Questionnaire for Impulsive Compulsive Disorders in Parkinson's Disease- Rating Scale). Voxel-wise analysis of dopamine agonist-induced cerebral blood flow revealed group differences in mesocortical (ventromedial prefrontal cortex; insular cortex), mesolimbic (ventral striatum), and midbrain (SN; periaqueductal gray) regions.

Conclusions: These results indicate that dopamine agonist therapy can augment mesocorticolimbic and striato-nigro-striatal network activity in patients susceptible to impulsive-compulsive behaviors. Our findings reinforce a wider literature linking studies of maladaptive behaviors to mesocorticolimbic networks and extend our understanding of biological mechanisms of impulsive compulsive behaviors in PD. © 2017 International Parkinson and Movement Disorder Society.

Keywords: Parkinson's disease; cerebral blood flow; dopamine; impulse control disorder; impulsive compulsive behaviors.

MeSH terms

  • Aged
  • Animals
  • Cerebral Cortex* / blood supply
  • Cerebral Cortex* / diagnostic imaging
  • Cerebral Cortex* / drug effects
  • Cerebrovascular Circulation / drug effects*
  • Dopamine Agonists / adverse effects*
  • Female
  • Humans
  • Impulsive Behavior / drug effects*
  • Impulsive Behavior / physiology
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Parkinson Disease / diagnostic imaging
  • Parkinson Disease / drug therapy*
  • Parkinson Disease / physiopathology
  • Periaqueductal Gray* / blood supply
  • Periaqueductal Gray* / diagnostic imaging
  • Periaqueductal Gray* / drug effects
  • Severity of Illness Index
  • Spin Labels
  • Ventral Striatum* / blood supply
  • Ventral Striatum* / chemistry
  • Ventral Striatum* / diagnostic imaging
  • Ventral Striatum* / drug effects

Substances

  • Dopamine Agonists
  • Spin Labels