Abstract
Recent imaging studies with the stop-signal task in healthy individuals indicate that the subthalamic nucleus, the pre-supplementary motor area and the inferior frontal gyrus are key components of the right hemisphere “inhibitory network”. Limited information is available regarding neural substrates of inhibitory processing in patients with asymmetric Parkinson’s disease. The aim of the current fMRI study was to identify the neural changes underlying deficient inhibitory processing on the stop-signal task in patients with predominantly left-sided Parkinson’s disease. Fourteen patients and 23 healthy controls performed a stop-signal task with the left and right hands. Behaviorally, patients showed delayed response inhibition with either hand compared to controls. We found small imaging differences for the right hand, however for the more affected left hand when behavior was successfully inhibited we found reduced activation of the inferior frontal gyrus bilaterally and the insula. Using the stop-signal delay as regressor, contralateral underactivation in the right dorsolateral prefrontal cortex, inferior frontal and anterior putamen were found in patients. This finding indicates dysfunction of the right inhibitory network in left-sided Parkinson’s disease. Functional connectivity analysis of the left subthalamic nucleus showed a significant increase of connectivity with bilateral insula. In contrast, the right subthalamic nucleus showed increased connectivity with visuomotor and sensorimotor regions of the cerebellum. We conclude that altered inhibitory control in left-sided Parkinson’s disease is associated with reduced activation in regions dedicated to inhibition in healthy controls, which requires engagement of additional regions, not observed in controls, to successfully stop ongoing actions.
Highlights
MethodsPatients with Parkinson’s disease (PD) have delayed motor inhibition relative to age-matched controls on the standard [Gauggel et al, 2004] and the conditional [Obeso et al, 2011a] versions of the stop-signal reaction time task (SSRT)
Correct inhibition was achieved at 61% (LPD patients) and 68% probabilities without statistical differences between groups (Table 2; z = -1.33, p = 0.18) and both showing expected cumulative probabilities to fail stopping as stop-signal delay (SSD) values increased
To further identify the brain areas activated in relation to motor inhibition subtracting the motor component, we examined the Stop-Inhibit-Go contrast controlling for response initiation involved on Go trials
Summary
MethodsPatients with Parkinson’s disease (PD) have delayed motor inhibition relative to age-matched controls on the standard [Gauggel et al, 2004] and the conditional [Obeso et al, 2011a] versions of the stop-signal reaction time task (SSRT). A key finding relevant to the current study was the demonstration in healthy participants that successful stopping was associated with significant activation of a right-hemispheric network involving the inferior frontal cortex (IFC), subthalamic nucleus (STN) and pre-SMA [Aron and Poldrack, 2006]. Inhibition depends primarily on a right-hemispheric network in healthy participants [Aron et al, 2007; Garavan et al, 1999; Hampshire et al, 2010; Ray Li et al, 2008; Rubia et al, 2003], that when perturbed recruit alternative regions [Obeso et al, 2013; Zandbelt et al, 2013]. Patients with right frontal lobe lesions [Aron et al, 2003] or left inferior frontal gyrus [Swick et al, 2008] and PD patients after right subthalamotomy [Obeso et al, 2014a] show impaired inhibitory control on the stop-signal task
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