Abstract
Clinical apathy results in dysfunction of goal directed behaviour, a key component of which is the initiation of action. Previous work has suggested that blunting of reward sensitivity is an important mechanism underlying apathy. However, an additional component might be impoverished initiation of action itself. This study aims to investigate the link between motivation and motor output and its association with apathy and dopamine. An oculomotor task that measures pupillary and saccadic response to monetary incentives was used to assess reward sensitivity, first in 23 young and 18 elderly controls, and then in 22 patients with Parkinson’s disease tested ON and OFF dopaminergic medication. To distinguish between pupillary responses to anticipated reward alone versus responses associated with motor preparation, a saccadic ‘go/no-go’ task was performed. Half of the trials required a saccade to be initiated to receive a reward and in the remaining trials no action was required but reward was still obtained. No significant difference in pupil response was demonstrated between the two conditions in all groups tested, suggesting pupillary responses to rewards are not contingent upon motor preparation in Parkinson’s disease. Being ON or OFF dopamine did not influence this response either. Previous work demonstrated associations between apathy and pupillary reward insensitivity in Parkinson’s disease. Here we observed this effect only when an action was required to receive a reward, and only in the ON state. These findings suggest that apathy in Parkinson’s disease is linked to reduced reward sensitivity and that this is most prominently observed when actions have to be initiated to rewarding goals, with the effect modulated by being ON dopaminergic medication. OFF medication, there was no such strong relationship, and similarly in the ‘no-go’ conditions, either ON or OFF dopaminergic drugs. The results provide preliminary data which suggest that apathy in Parkinson’s disease is associated with a reduction in reward sensitivity and this is most evident when associated with initiation of goal directed actions in the presence of adequate dopamine.
Highlights
IntroductionClinical apathy is a syndrome which manifests as a reduction in goal directed behaviour and is associated with significant reduction in quality of life.[1,2,3,4,5,6] It is common in neurodegenerative disorders, Parkinson’s disease with a prevalence ranging up to 70%.7–12 Importantly, apathy is considered not to be a secondary psychological reaction to physical impairments of Parkinson’s disease,[8] but instead a consequence of neurodegeneration of frontostriatal regions, including reward sensitive regions of the basal ganglia, such as the ventral striatum, and the dorsal anterior cingulate cortex—areas that play a central role in motivated behaviour and initiation of actions.[13]Over the last few years, several studies have suggested blunted reward sensitivity forms an important component of apathy
We aim to address the following questions: First, do anticipatory pupil responses to rewards arise due to motor preparation signals linked to performing an action, or are such anticipatory pupil responses to reward dissociable from movement? Second, are reward sensitivity deficits in Parkinson’s disease patients with clinical apathy linked to impairments in the evaluation of rewards only or, are the initiation of actions crucial for association of reward cues? how are anticipatory pupillary responses associated with or without actions, modulated by dopaminergic state in Parkinson’s disease?
Parkinson’s disease patients were assessed for apathy using the Lille Apathy Rating Scale (LARS)[41]; they were screened for depression with the Beck Depression Inventory-II (BDI-II)[42] and for cognitive impairment using the Montreal Cognitive Assessment (MoCA).[43]
Summary
Clinical apathy is a syndrome which manifests as a reduction in goal directed behaviour and is associated with significant reduction in quality of life.[1,2,3,4,5,6] It is common in neurodegenerative disorders, Parkinson’s disease with a prevalence ranging up to 70%.7–12 Importantly, apathy is considered not to be a secondary psychological reaction to physical impairments of Parkinson’s disease,[8] but instead a consequence of neurodegeneration of frontostriatal regions, including reward sensitive regions of the basal ganglia, such as the ventral striatum, and the dorsal anterior cingulate cortex—areas that play a central role in motivated behaviour and initiation of actions.[13]Over the last few years, several studies have suggested blunted reward sensitivity forms an important component of apathy. The association with reward sensitivity and apathy has been demonstrated in Parkinson’s disease and found to be modulated by dopamine. This has been explored using different behavioural paradigms, including effort-based decision-making tasks and oculomotor eye tracking experiments.[14,15,16,17] Results from reward-effort discounting assessments demonstrate Parkinson’s disease patients with apathy are less inclined to make a physical effort for reward compared to those without apathy, if the reward level is low.[17] dopamine therapy in these patients increases both motor vigour and engagement rate for high effort and higher offer rewards, highlighting dopamine’s modulatory effect
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