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. 2017 Feb 13;12(2):e0172019.
doi: 10.1371/journal.pone.0172019. eCollection 2017.

Does dystonic muscle activity affect sense of effort in cervical dystonia?

Loïc Carment  1 , Marc A Maier  1   2 , Sophie Sangla  3 , Vincent Guiraud  4   5 , Serge Mesure  6 , Marie Vidailhet  7   8 , Påvel G Lindberg  1   9 , Jean-Pierre Bleton  3
Affiliations

Does dystonic muscle activity affect sense of effort in cervical dystonia?

Loïc Carment et al. PLoS One. .

Abstract

Background: Focal dystonia has been associated with deficient processing of sense of effort cues. However, corresponding studies are lacking in cervical dystonia (CD). We hypothesized that dystonic muscle activity would perturb neck force control based on sense of effort cues.

Methods: Neck extension force control was investigated in 18 CD patients with different clinical features (7 with and 11 without retrocollis) and in 19 control subjects. Subjects performed force-matching and force-maintaining tasks at 5% and 20% of maximum voluntary contraction (MVC). Three task conditions were tested: i) with visual force feedback, ii) without visual feedback (requiring use of sense of effort), iii) without visual feedback, but with neck extensor muscle vibration (modifying muscle afferent cues). Trapezius muscle activity was recorded using electromyography (EMG).

Results: CD patients did not differ in task performance from healthy subjects when using visual feedback (ANOVA, p>0.7). In contrast, when relying on sense of effort cues (without visual feedback, 5% MVC), force control was impaired in patients without retrocollis (p = 0.006), but not in patients with retrocollis (p>0.2). Compared to controls, muscle vibration without visual feedback significantly affected performance in patients with retrocollis (p<0.001), but not in patients without retrocollis. Extensor EMG during rest, included as covariate in ANOVA, explained these group differences.

Conclusion: This study shows that muscle afferent feedback biases sense of effort cues when controlling neck forces in patients with CD. The bias acts on peripheral or central sense of effort cues depending on whether the task involves dystonic muscles. This may explain why patients with retrocollis more accurately matched isometric neck extension forces. This highlights the need to consider clinical features (pattern of dystonic muscles) when evaluating sensorimotor integration in CD.

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Conflict of interest statement

LC reports grants from Université Pierre et Marie Curie, Paris VI, outside the submitted work. SS reports personal fees from Allergan, personal fees from Ipsen, personal fees from Merz-Pharma, outside the submitted work. VG has nothing to disclose. SM reports grants from Fondation Paul Bennetot, outside the submitted work. MV reports grants from INSERM, grants from APHP, grants from APTES, grants from France Parkinson, grants from AMADYS, personal fees from Movement Disorders Society, outside the submitted work; and Member of the advisory board for Merz and Medtronic. PGL reports grants from Gloria and Jacques Gosweiler Foundation, outside the submitted work and owns shares in Aggero MedTech AB, a company commercializing a measurement instrument for spasticity. In addition, PGL and MAM have patented a method for measurement of manual dexterity (EP2659835A1). JPB reports personal fees from MERZ-PHARMA, personal fees from IPSEN, grants from AMADYS, grants from AFREK, outside the submitted work. This does not alter the authors’ adherence to PLOS ONE policies on sharing data and materials.

Figures

Fig 1
Fig 1. Setup and visuomotor tasks.
(A) Setup for visuomotor tasks. Subjects were seated in front of a computer screen. A headband was attached to the force sensor by a non-extensible wire. The task consisted of a series (trials) of visually displayed target forces (height of white rectangle) to be matched as closely as possible using visual feedback of the exerted neck force (height of red rectangle). (B) Force matching task: subjects matched the neck extension force to an indicated target level (5% or 20% MVC) with visual force feedback (condition_Vis) and reproduced the same force level without visual feedback (condition_NoVis). In conditions without vision, subjects were given an auditory cue indicating force onset, offset or hold. Five trials/condition were presented in a pseudo-randomized order. Force exerted during the stable part of the hold phase, indicated by grey shading, was analyzed. (C) Force-maintaining task: subjects maintained their extension force at target level with visual feedback (condition_Vis). The visual feedback was then removed for six seconds (condition_NoVis) and vibration was applied (condition_NoVis+Vib).
Fig 2
Fig 2. Comparison of raw data for a control subject, a CD_R- and a CD_R+ patient.
(A) Control subject: raw data recorded during the force matching task at 5% MVC and 20% MVC: Neck extension force was first down-sampled (100Hz) and normalized for each subject to the target force level (NU: normalized units). Lower trace: EMG activity of right trapezius (TPZ). Example trials show force and EMG traces during condition_Vis, condition_NoVis, and condition_ NoVis+Vib. Note: EMG was not recorded during vibration. (B) CD_R- patient: corresponding examples. (C) CD_R+ patient: corresponding examples.
Fig 3
Fig 3. Group performance in the visuomotor force-matching task.
Mean force (mean±SD) for the three groups during condition_Vis, condition_NoVis and condition_NoVis+Vib at 5% MVC (A) and at 20% MVC (B). (A) No significant difference in mean force between groups in condition_Vis. Significant differences at 5% MVC during condition_NoVis between CD_R- and control subjects (p = 0.006), and also between CD_R- and CD_R+ patients (p = 0.002). Note that the variability of mean force (SD) increased about 5-fold in all three groups. Significant differences during condition_NoVis+Vib between CD_R+ and control subjects (p = 0.006) and also between CD_R+ and CD_R- patients (p<0.001). (B) No difference in mean force at 20% MVC. * = p<0.05; ** = p<0.01; *** = p<0.001.
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References

    1. Albanese A, Bhatia K, Bressman SB, Delong MR, Fahn S, Fung VSC, et al. Phenomenology and classification of dystonia: a consensus update. Mov Disord. 2013. June 15;28(7):863–73. 10.1002/mds.25475 - DOI - PMC - PubMed
    1. Avanzino L, Tinazzi M, Ionta S, Fiorio M. Sensory-motor integration in focal dystonia. Neuropsychologia. 2015. December;79(Pt B):288–300. 10.1016/j.neuropsychologia.2015.07.008 - DOI - PubMed
    1. Bleton J-P, Teremetz M, Vidailhet M, Mesure S, Maier MA, Lindberg PG. Impaired force control in writer’s cramp showing a bilateral deficit in sensorimotor integration. Mov Disord. 2014. January;29(1):130–4. 10.1002/mds.25690 - DOI - PubMed
    1. Proske U, Gandevia SC. The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev. 2012. October;92(4):1651–97. 10.1152/physrev.00048.2011 - DOI - PubMed
    1. Boccagni C, Carpaneto J, Micera S, Bagnato S, Galardi G. Motion analysis in cervical dystonia. Neurol Sci. 2008. December;29(6):375–81. - PubMed