Sequence effect in Parkinson’s disease is related to motor energetic cost

Bradykinesia is the most disabling motor symptom of Parkinson’s disease (PD). The sequence effect, a feature of bradykinesia, refers to the rapid decrement in amplitude and speed of repetitive movements (e.g., gait, handwriting) and is a major cause of morbidity in PD. Previous research has revealed...

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Main Authors: Sule eTinaz, Ajay S Pillai, Mark eHallett
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-05-01
Series:Frontiers in Neurology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fneur.2016.00083/full
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spelling doaj-877ea8b39b5841928e2c0d72be0f20092020-11-24T23:07:08ZengFrontiers Media S.A.Frontiers in Neurology1664-22952016-05-01710.3389/fneur.2016.00083198819Sequence effect in Parkinson’s disease is related to motor energetic costSule eTinaz0Sule eTinaz1Ajay S Pillai2Mark eHallett3Yale School of MedicineNational Institute of Neurological Disorders and Stroke, National Institutes of HealthNational Institute of Neurological Disorders and Stroke, National Institutes of HealthNational Institute of Neurological Disorders and Stroke, National Institutes of HealthBradykinesia is the most disabling motor symptom of Parkinson’s disease (PD). The sequence effect, a feature of bradykinesia, refers to the rapid decrement in amplitude and speed of repetitive movements (e.g., gait, handwriting) and is a major cause of morbidity in PD. Previous research has revealed mixed results regarding the role of dopaminergic treatment in the sequence effect. However, external cueing has been shown to improve it. In this study, we aimed to characterize the sequence effect systematically and relate this phenomenon to the energetic cost of movement within the context of cost-benefit framework of motor control. We used a dynamic isometric motor task with auditory pacing to assess the sequence effect in motor output during a 15 s task segment in PD patients and matched controls. All participants performed the task with both hands, and without and with visual feedback. Patients were also tested in on- and off-dopaminergic states. Patients in the off state did not show higher sequence effect compared to controls, partly due to large variance in their performance. However, patients in the on state and in the absence of visual feedback, showed significantly higher sequence effect compared to controls. Patients expended higher total motor energy compared to controls in all conditions and regardless of their medication status. In this experimental situation, the sequence effect in PD is associated with the cumulative energetic cost of movement. Dopaminergic treatment, critical for internal triggering of movement, fails to maintain the motor vigor across responses. The high motor cost may be related to failure to incorporate limbic/motivational cues into the motor plan. Visual feedback may facilitate performance by shifting the driving of movement from internal to external, or, alternatively, by functioning as a motivational cue.http://journal.frontiersin.org/Journal/10.3389/fneur.2016.00083/fullDopamineFatiguemotor controlvisual feedbackbradykinesiacost-benefit
collection DOAJ
language English
format Article
sources DOAJ
author Sule eTinaz
Sule eTinaz
Ajay S Pillai
Mark eHallett
spellingShingle Sule eTinaz
Sule eTinaz
Ajay S Pillai
Mark eHallett
Sequence effect in Parkinson’s disease is related to motor energetic cost
Frontiers in Neurology
Dopamine
Fatigue
motor control
visual feedback
bradykinesia
cost-benefit
author_facet Sule eTinaz
Sule eTinaz
Ajay S Pillai
Mark eHallett
author_sort Sule eTinaz
title Sequence effect in Parkinson’s disease is related to motor energetic cost
title_short Sequence effect in Parkinson’s disease is related to motor energetic cost
title_full Sequence effect in Parkinson’s disease is related to motor energetic cost
title_fullStr Sequence effect in Parkinson’s disease is related to motor energetic cost
title_full_unstemmed Sequence effect in Parkinson’s disease is related to motor energetic cost
title_sort sequence effect in parkinson’s disease is related to motor energetic cost
publisher Frontiers Media S.A.
series Frontiers in Neurology
issn 1664-2295
publishDate 2016-05-01
description Bradykinesia is the most disabling motor symptom of Parkinson’s disease (PD). The sequence effect, a feature of bradykinesia, refers to the rapid decrement in amplitude and speed of repetitive movements (e.g., gait, handwriting) and is a major cause of morbidity in PD. Previous research has revealed mixed results regarding the role of dopaminergic treatment in the sequence effect. However, external cueing has been shown to improve it. In this study, we aimed to characterize the sequence effect systematically and relate this phenomenon to the energetic cost of movement within the context of cost-benefit framework of motor control. We used a dynamic isometric motor task with auditory pacing to assess the sequence effect in motor output during a 15 s task segment in PD patients and matched controls. All participants performed the task with both hands, and without and with visual feedback. Patients were also tested in on- and off-dopaminergic states. Patients in the off state did not show higher sequence effect compared to controls, partly due to large variance in their performance. However, patients in the on state and in the absence of visual feedback, showed significantly higher sequence effect compared to controls. Patients expended higher total motor energy compared to controls in all conditions and regardless of their medication status. In this experimental situation, the sequence effect in PD is associated with the cumulative energetic cost of movement. Dopaminergic treatment, critical for internal triggering of movement, fails to maintain the motor vigor across responses. The high motor cost may be related to failure to incorporate limbic/motivational cues into the motor plan. Visual feedback may facilitate performance by shifting the driving of movement from internal to external, or, alternatively, by functioning as a motivational cue.
topic Dopamine
Fatigue
motor control
visual feedback
bradykinesia
cost-benefit
url http://journal.frontiersin.org/Journal/10.3389/fneur.2016.00083/full
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