Dopamine and eye movement control in Parkinson's disease: deficits in corollary discharge signals?

PeerJ. 2018 Dec 7:6:e6038. doi: 10.7717/peerj.6038. eCollection 2018.

Abstract

Movement in Parkinson's disease (PD) is fragmented, and the patients depend on visual information in their behavior. This suggests that the patients may have deficits in internally monitoring their own movements. Internal monitoring of movements is assumed to rely on corollary discharge signals that enable the brain to predict the sensory consequences of actions. We studied early-stage PD patients (N = 14), and age-matched healthy control participants (N = 14) to examine whether PD patients reveal deficits in updating their sensory representations after eye movements. The participants performed a double-saccade task where, in order to accurately fixate a second target, the participant must correct for the displacement caused by the first saccade. In line with previous reports, the patients had difficulties in fixating the second target when the eye movement was performed without visual guidance. Furthermore, the patients had difficulties in taking into account the error in the first saccade when making a saccade toward the second target, especially when eye movements were made toward the side with dominant motor symptoms. Across PD patients, the impairments in saccadic eye movements correlated with the integrity of the dopaminergic system as measured with [123I]FP-CIT SPECT: Patients with lower striatal (caudate, anterior putamen, and posterior putamen) dopamine transporter binding made larger errors in saccades. This effect was strongest when patients made memory-guided saccades toward the second target. Our results provide tentative evidence that the motor deficits in PD may be partly due to deficits in internal monitoring of movements.

Keywords: Corollary discharge; Dopamine; Dopamine transporter binding; Efference copy; Parkinson’s disease; Predictive coding; Saccadic eye movement.

Grants and funding

Henry Railo was funded by Turku Institute of Advanced Studies and Academy of Finland (grant #308533), and received a grant from the Finnish Cultural Foundation. Henri Olkoniemi was funded by the Finnish Cultural Foundation. Juho Joutsa was funded by the Academy of Finland (grant # 295580), the Finnish Medical Foundation and the Orion Research Foundation, and has received travel grants from Orion and Abbvie, and a research grant from Lundbeck. Valtteri Kaasinen was funded by the Turku University Hospital (ERVA-funds). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.