Characteristics of Rest and Postural Tremors in Parkinson’s Disease: An Analysis of Motor Unit Firing Synchrony and Patterns
The neural mechanisms responsible for resting and postural tremor in Parkinson’s disease (PD) have been the object of considerable study, much of it focusing on supraspinal sites. Here, we adopted an alternative approach that emphasizes motor unit (MU) firing synchrony and patterns of discharge. To...
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doaj-660dd5290c5e437f9badcfacd0d89e392020-11-25T02:53:13ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612018-05-011210.3389/fnhum.2018.00179322767Characteristics of Rest and Postural Tremors in Parkinson’s Disease: An Analysis of Motor Unit Firing Synchrony and PatternsOrsalia M. Agapaki0Orsalia M. Agapaki1Constantinos N. Christakos2Constantinos N. Christakos3Dimitrios Anastasopoulos4Dimitrios Anastasopoulos5Laboratory of Systems Physiology, Division of Basic Sciences, Medical School, University of Crete, Heraklion, GreeceComputational Neuroscience Group, Institute of Applied and Computational Mathematics, Foundation for Research and Technology – Hellas, Heraklion, GreeceLaboratory of Systems Physiology, Division of Basic Sciences, Medical School, University of Crete, Heraklion, GreeceComputational Neuroscience Group, Institute of Applied and Computational Mathematics, Foundation for Research and Technology – Hellas, Heraklion, GreeceLaboratory of Physiology and Clinical Neurophysiology, School of Nursing, National and Kapodistrian University of Athens, Athens, GreeceDepartment of Neurology, Medical School, University of Ioannina, Ioannina, GreeceThe neural mechanisms responsible for resting and postural tremor in Parkinson’s disease (PD) have been the object of considerable study, much of it focusing on supraspinal sites. Here, we adopted an alternative approach that emphasizes motor unit (MU) firing synchrony and patterns of discharge. To explore if these could account for known features of PD tremor, we recorded the instantaneous acceleration of the upper limb of 23 PD patients at rest or while they tried to hold a stable posture together with surface EMG and single MU discharges of upper limb muscles. Spectral, coherence and cross-correlation analyses of the recorded signals demonstrated alternating epoch-I and epoch-II intervals in PD patients both at rest and while they held a stable posture. Epoch-II intervals are characterized by the presence of 4–8 Hz overt tremor, enhanced MU synchrony and spike-doublets or triplets bearing a one-to-one relation to each tremor cycle. Epoch-I resembled physiological tremor in that it was characterized by 6–10 Hz non-overt tremor, lower MU synchrony and rhythmical MU firing at the intrinsic rate of the unit. The frequency of overt and non-overt tremor remained the same whether the patient was at rest or held a stable posture and the same was true of the remaining characteristics of epoch-I and epoch-II. The mean interval between spikes of a doublet/triplet varied between 30 and 50 ms and, for any given patient, remained roughly constant throughout measurements. This is the first time that enhanced MU synchrony and spike doublets/triplets characterized by relatively stable interspike intervals, are shown to accompany the overt tremor of PD patients. To account for our findings we propose that a two-state oscillatory spinal stretch reflex loop generates overt parkinsonian tremor in response to intermittent, descending, relatively high frequency oscillatory signals.http://journal.frontiersin.org/article/10.3389/fnhum.2018.00179/fullParkinsonian tremormotor unit spike doublets/tripletsspectral analysiscorrelation analysissynchronyspinal stretch reflex |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Orsalia M. Agapaki Orsalia M. Agapaki Constantinos N. Christakos Constantinos N. Christakos Dimitrios Anastasopoulos Dimitrios Anastasopoulos |
spellingShingle |
Orsalia M. Agapaki Orsalia M. Agapaki Constantinos N. Christakos Constantinos N. Christakos Dimitrios Anastasopoulos Dimitrios Anastasopoulos Characteristics of Rest and Postural Tremors in Parkinson’s Disease: An Analysis of Motor Unit Firing Synchrony and Patterns Frontiers in Human Neuroscience Parkinsonian tremor motor unit spike doublets/triplets spectral analysis correlation analysis synchrony spinal stretch reflex |
author_facet |
Orsalia M. Agapaki Orsalia M. Agapaki Constantinos N. Christakos Constantinos N. Christakos Dimitrios Anastasopoulos Dimitrios Anastasopoulos |
author_sort |
Orsalia M. Agapaki |
title |
Characteristics of Rest and Postural Tremors in Parkinson’s Disease: An Analysis of Motor Unit Firing Synchrony and Patterns |
title_short |
Characteristics of Rest and Postural Tremors in Parkinson’s Disease: An Analysis of Motor Unit Firing Synchrony and Patterns |
title_full |
Characteristics of Rest and Postural Tremors in Parkinson’s Disease: An Analysis of Motor Unit Firing Synchrony and Patterns |
title_fullStr |
Characteristics of Rest and Postural Tremors in Parkinson’s Disease: An Analysis of Motor Unit Firing Synchrony and Patterns |
title_full_unstemmed |
Characteristics of Rest and Postural Tremors in Parkinson’s Disease: An Analysis of Motor Unit Firing Synchrony and Patterns |
title_sort |
characteristics of rest and postural tremors in parkinson’s disease: an analysis of motor unit firing synchrony and patterns |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Human Neuroscience |
issn |
1662-5161 |
publishDate |
2018-05-01 |
description |
The neural mechanisms responsible for resting and postural tremor in Parkinson’s disease (PD) have been the object of considerable study, much of it focusing on supraspinal sites. Here, we adopted an alternative approach that emphasizes motor unit (MU) firing synchrony and patterns of discharge. To explore if these could account for known features of PD tremor, we recorded the instantaneous acceleration of the upper limb of 23 PD patients at rest or while they tried to hold a stable posture together with surface EMG and single MU discharges of upper limb muscles. Spectral, coherence and cross-correlation analyses of the recorded signals demonstrated alternating epoch-I and epoch-II intervals in PD patients both at rest and while they held a stable posture. Epoch-II intervals are characterized by the presence of 4–8 Hz overt tremor, enhanced MU synchrony and spike-doublets or triplets bearing a one-to-one relation to each tremor cycle. Epoch-I resembled physiological tremor in that it was characterized by 6–10 Hz non-overt tremor, lower MU synchrony and rhythmical MU firing at the intrinsic rate of the unit. The frequency of overt and non-overt tremor remained the same whether the patient was at rest or held a stable posture and the same was true of the remaining characteristics of epoch-I and epoch-II. The mean interval between spikes of a doublet/triplet varied between 30 and 50 ms and, for any given patient, remained roughly constant throughout measurements. This is the first time that enhanced MU synchrony and spike doublets/triplets characterized by relatively stable interspike intervals, are shown to accompany the overt tremor of PD patients. To account for our findings we propose that a two-state oscillatory spinal stretch reflex loop generates overt parkinsonian tremor in response to intermittent, descending, relatively high frequency oscillatory signals. |
topic |
Parkinsonian tremor motor unit spike doublets/triplets spectral analysis correlation analysis synchrony spinal stretch reflex |
url |
http://journal.frontiersin.org/article/10.3389/fnhum.2018.00179/full |
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