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February 11, 2020; 94 (6) Article

Tactile and proprioceptive dysfunction differentiates cervical dystonia with and without tremor

Laura Avanzino, Amel Cherif, View ORCID ProfileOscar Crisafulli, Federico Carbone, Jacopo Zenzeri, Pietro Morasso, Giovanni Abbruzzese, Elisa Pelosin, Jürgen Konczak
First published January 14, 2020, DOI: https://doi.org/10.1212/WNL.0000000000008916
Laura Avanzino
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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Amel Cherif
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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Oscar Crisafulli
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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  • ORCID record for Oscar Crisafulli
Federico Carbone
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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Jacopo Zenzeri
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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Pietro Morasso
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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Giovanni Abbruzzese
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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Elisa Pelosin
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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Jürgen Konczak
From the Department of Experimental Medicine (L.A.), Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, Department of Informatics, Bioengineering, Robotics and System Engineering (A.C.), and Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal Child Health (O.C., F.C., G.A., E.P.), University of Genova; Ospedale Policlinico San Martino (L.A., E.P.), IRCCS; Robotics, Brain and Cognitive Sciences Department (A.C., J.Z., P.M.), Istituto Italiano di Tecnologia, Genoa, Italy; and Human Sensorimotor Control Laboratory (J.K.), Center for Clinical Movement Science and School of Kinesiology, University of Minnesota, Minneapolis.
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Tactile and proprioceptive dysfunction differentiates cervical dystonia with and without tremor
Laura Avanzino, Amel Cherif, Oscar Crisafulli, Federico Carbone, Jacopo Zenzeri, Pietro Morasso, Giovanni Abbruzzese, Elisa Pelosin, Jürgen Konczak
Neurology Feb 2020, 94 (6) e639-e650; DOI: 10.1212/WNL.0000000000008916

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Abstract

Objective To determine whether different phenotypes of cervical dystonia (CD) express different types and levels of somatosensory impairment.

Methods We assessed somatosensory function in patients with CD with and without tremor (n = 12 each) and in healthy age-matched controls (n = 22) by measuring tactile temporal discrimination thresholds of the nondystonic forearm and proprioceptive acuity in both the dystonic (head/neck) and nondystonic body segments (forearm/hand) using a joint position‐matching task. The head or the wrist was passively displaced along different axes to distinct joint positions by the experimenter or through a robotic exoskeleton. Participants actively reproduced the experienced joint position, and the absolute joint position‐matching error between the target and the reproduced positions served as a marker of proprioceptive acuity.

Results Tactile temporal discrimination thresholds were significantly elevated in both CD subgroups compared to controls. Proprioceptive acuity of both the dystonic and nondystonic body segments was elevated in patients with CD and tremor with respect to both healthy controls and patients with CD without tremor. That is, tactile abnormalities were a shared dysfunction of both CD phenotypes, while proprioceptive dysfunction was observed in patients with CD with tremor.

Conclusions Our findings suggest that the pathophysiology in CD can be characterized by 2 abnormal neural processes: a dysfunctional somatosensory gating mechanism involving the basal ganglia that triggers involuntary muscle spasms and abnormal processing of proprioceptive information within a defective corticocerebellar loop, likely affecting the feedback and feedforward control of head positioning. This dysfunction is expressed mainly in CD with tremor.

Glossary

Abd/Add=
abduction/adduction;
CD=
cervical dystonia;
CD-NT=
cervical dystonia without tremor;
CD-T=
cervical dystonia with tremor;
Flex/Ext=
flexion/extension;
HC=
healthy controls;
ISI=
interstimulus interval;
PAI=
proprioceptive acuity index;
PS=
pronation/supination;
RM-ANCOVA=
repeated-measures analysis of covariance;
RoM=
range of motion;
TDt=
temporal discrimination thresholds

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • Editorial, page 243

  • Received May 16, 2019.
  • Accepted in final form August 28, 2019.
  • © 2020 American Academy of Neurology
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