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Biased Visuospatial Attention in Cervical Dystonia

Published online by Cambridge University Press:  09 August 2017

Gaetana Chillemi*
Affiliation:
Department of Clinical and Experimental Medicine, Messina, Italy
Caterina Formica
Affiliation:
Department of Clinical and Experimental Medicine, Messina, Italy
Adriana Salatino
Affiliation:
Department of Psychology, University of Torino, Torino, Italy
Alessandro Calamuneri
Affiliation:
Department of Clinical and Experimental Medicine, Messina, Italy
Paolo Girlanda
Affiliation:
Department of Clinical and Experimental Medicine, Messina, Italy
Francesca Morgante
Affiliation:
Department of Clinical and Experimental Medicine, Messina, Italy
Demetrio Milardi
Affiliation:
IRCCS Centro Neurolesi “Bonino Pulejo”, S.S. 113, Messina, Italy Department of Biomedical and Dental Sciences and Morphofunctional Imaging, University of Messina, Messina, Italy
Carmen Terranova
Affiliation:
Department of Clinical and Experimental Medicine, Messina, Italy
Alberto Cacciola
Affiliation:
IRCCS Centro Neurolesi “Bonino Pulejo”, S.S. 113, Messina, Italy
Angelo Quartarone
Affiliation:
IRCCS Centro Neurolesi “Bonino Pulejo”, S.S. 113, Messina, Italy Department of Biomedical and Dental Sciences and Morphofunctional Imaging, University of Messina, Messina, Italy
Raffaella Ricci
Affiliation:
Department of Psychology, University of Torino, Torino, Italy
*
Correspondence and reprint requests to: Gaetana Chillemi, Clinica Neurologica 2, Policlinico Universitario, 98125 Messina, Italy. E-mail: [email protected]

Abstract

Objectives: There is increasing evidence of non-motor, sensory symptoms, mainly involving the spatial domain, in cervical dystonia (CD). These manifestations are likely driven by dysfunctional overactivity of the parietal cortex during the execution of a sensory task. Few studies also suggest the possibility that visuospatial attention might be specifically affected in patients with CD. Therefore, we asked whether non-motor manifestations in CD might also comprise impairment of higher level visuospatial processing. Methods: To this end, we investigated visuospatial attention in 23 CD patients and 12 matched healthy controls (for age, gender, education, and ocular dominance). The patients were identified according to the dystonia pattern type (laterocollis vs. torticollis). Overall, participants were right-handers, and the majority of them was right-eye dominant. Visuospatial attention was assessed using a line bisection task. Participants were asked to bisect horizontal lines, using their right or left hand. Results: Participants bisected more to the left of true center when using their left hand to perform the task than when using their right hand. However, overall, torticollis patients produced a significantly greater leftward deviation than controls. Conclusions: These data are consistent with preliminary findings suggesting the presence of biased spatial attention in patients with idiopathic cervical dystonia. The presence of an attentional bias in patients with torticollis seem to indicate that alterations of attentional circuits might be implicated in the pathophysiology of this type of CD. (JINS, 2018, 24, 23–32)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

Albanese, A., Bhatia, K., Bressman, S.B., Delong, M.R., Fahn, S., Fung, V.S., & Teller, J.K. (2013). Phenomenology and classification of dystonia: A consensus update. Movement Disorders, 28(7), 863873.Google Scholar
Allam, N., Frank, J.E., Pereira, C., & Tomaz, C. (2007). Sustained attention in cranial dystonia patients treated with botulinum toxin. Acta Neurologica Scandinavica Journal, 116(3), 196200.Google Scholar
Bagiella, E., Sloan, R.P., & Heitjan, D.F. (2000). Mixed effects models in psychophysiology. Psychophysiology, 37(1), 1320.CrossRefGoogle ScholarPubMed
Bares, M., Lungu, O., Liu, T., Waechter, T., Gomez, C.M., & Ashe, J. (2007). Impaired predictive motor timing in patients with cerebellar disorders. Experimental Brain Research, 180(2), 355365.CrossRefGoogle ScholarPubMed
Bares, M., Lungu, O.V., Husárová, I., & Gescheidt, T. (2010). Predictive motor timing performance dissociates between early diseases of the cerebellum and Parkinson’s disease. Cerebellum, 9(1), 124135.CrossRefGoogle ScholarPubMed
Bares, M., Lungu, O.V., Liu, T., Waechter, T., Gomez, C.M., & Ashe, J. (2011). The neural substrate of predictive motor timing in spinocerebellar ataxia. Cerebellum, 10(2), 233244.Google Scholar
Benwell, C.S.Y., Thut, G., Grant, A., & Harvey, M. (2014). A rightward shift in the visuospatial attention vector with healthy aging. Frontiers in Aging Neuroscience, 6(113), 111.CrossRefGoogle ScholarPubMed
Bowers, D., & Heilman, K.M. (1980). Pseudoneglect: Effects of hemispace on a tactile line bisection task. Neuropsychologia, 18(4–5), 491498.CrossRefGoogle ScholarPubMed
Brashear, A. (2004). Treatment of cervical dystonia with botulinum toxin. Operative Techniques in Otolaryngology—Head and Neck Surgery, 15(2), 122127.Google Scholar
Caraceni, A., Mendoza, T.R., Mencaglia, E., Barbatella, C., Edwards, K., Forjaz, M.J., & Cleeland, C.S. (1996). A validation study of an Italian version of the Brief Pain Inventory (Breve Questionario Per La Valutazione Del Dolore). Pain, 65(1), 8792.CrossRefGoogle ScholarPubMed
Chan, J., Brin, M.F., Fahn, S. (1991). Idiopathic cervical dystonia: Clinical characteristics. Movement Disorders, 6(2), 119126. doi:10.1002/mds.870060206 Google Scholar
Chieffi, S., Lavarone, A., Iaccarino, L., La Marra, M., Messina, G., De Luca, V., & Monda, M. (2014). Age-related differences in distractor interference on line bisection. Experimental Brain Research, 232(11), 36593664.Google Scholar
Chillemi, G., Calamuneri, A., Morgante, F., Terranova, C., Rizzo, V, Girlanda, P., & Quartarone, A. (2017). A. spatial and temporal high processing of visual and auditory stimuli in cervical dystonia. Frontiers in Neurology, 8(1), 66.Google Scholar
Cho, H.J., & Hallett, M. (2016). Non-invasive brain stimulation for treatment of focal hand dystonia: Update and future direction. Journal of Movement Disorders, 9(2), 5562. doi: 10.14802/jmd.16014 Google Scholar
De Vries, P.M., De Jong, B.M., Bohning, D.E., Hinson, V.K., George, M.S., & Leenders, K.L. (2012). Reduced parietal activation in cervical dystonia after parietal TMS interleaved with fMRI. Clinical Neurology and Neurosurgery, 114(7), 914921.CrossRefGoogle ScholarPubMed
Duane, D.D. (1991). Treatment of spasmodic Torticollis. Mayo Clinic Proceedings, 66(9), 969971.Google Scholar
Fabbrini, G., Berardelli, I., Moretti, G., Pasquini, M., Bloise, M., Colosimo, C., & Berardelli, A. (2010). Psychiatric disorders in adult-onset focal dystonia: A case-control study. Movement Disorders, 25(4), 459465. doi: 10.1002/mds.22983 CrossRefGoogle ScholarPubMed
Filip, P., Lungu, O.V., Shaw, D.J., Kasparek, T., & Bares, M. (2013). The mechanisms of movement control and time estimation in cervical dystonia patients. Neural Plasticity, 2013(2013), 908741. doi: 10.1155/2013/908741 Google Scholar
Fink, G.R., Marshall, J.C., Shah, N.J., Weiss, P.H., Halligan, P.W., Grosse-Ruyken, M., & Freund, H.J. (2000). Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI. Neurology, 54, 13241331.Google Scholar
Finney, G.R., Williamson, J.B., Brandon Burtis, D., Drago, V., Mizuno, T., Jeong, Y., & Heilman, K.M. (2015). The effects of chronic right hemispheric damage on the allocation of spatial attention: Alterations of accuracy and reliability. Journal of the International Neuropsychological Society, 21(5), 373377.Google Scholar
Fukatsu, R., Fujii, T., Kimura, I., Saso, S., & Kogure, K. (1990). Effects of hand and spatial conditions on visual line bisection. The Tohoku Journal of Experimental Medicine, 161, 329333.CrossRefGoogle ScholarPubMed
Ghilardi, M.F., Carbon, M., Silvestri, G., Dhawan, V., Tagliati, M., Bressman, S., & Eidelberg, D. (2003). Impaired sequence learning in carriers of the DYT1 dystonia mutation. Annals of Neurology, 54(1), 102109.CrossRefGoogle ScholarPubMed
Hallett, M. (2011). Neurophysiology of dystonia: The role of inhibition. Neurobiology of Disease, 42(2), 177184.Google Scholar
Hinse, P., Leplow, B., Humbert, T., Lamparter, U., Junge, A., & Emskötter, T. (1996). Impairment of visuospatial function in idiopathic spasmodic Torticollis. Journal of Neurology, 243(1), 2933.Google Scholar
Husarova, I., Lungu, O.V., Marecek, R., Mikl, M., Gescheidt, T., Krupa, P., & Bares, M. (2011). Functional imaging of the cerebellum and basal ganglia during predictive motor timing in early Parkinson’s disease. Journal of Neuroimaging, 24(1), 4553.Google Scholar
Ishihara, M., Revol, P., Jacquin-Courtois, S., Mayet, R., Rode, G., Boisson, D., & Rossetti, Y. (2013). Tonal cues modulate line bisection performance: Preliminary evidence for a new rehabilitation prospect? Frontiers in Psychology, 4, 704.CrossRefGoogle ScholarPubMed
Jewell, G., & McCourt, M.E. (2000). Pseudoneglect: A review and meta-analysis of performance factors in line bisection tasks. Neuropsychologia, 38, 93110.Google Scholar
Kuoppamaki, M., Giunti, P., Quinn, N., Wood, N.W., & Bhatia, K.P. (2003). Slowly progressive cerebellar ataxia and cervical dystonia: Clinical presentation of a new form of spinocerebellar ataxia? Movement Disorders, 18(2), 200206.Google Scholar
Kuyper, D.J., Parra, V., Aerts, S., Okun, M.S., & Kluger, B.M. (2011). Nonmotor manifestations of dystonia: A systematic review. Movement Disorders, 26(7), 12061217.Google Scholar
Lange, F., Seer, C., Dengler, R., Dressler, D., & Kopp, B. (2016). Cognitive flexibility in primary dystonia. Journal of the International Neuropsychological Society, 22, 662670.CrossRefGoogle ScholarPubMed
Laudate, T.M., Neargarder, S., & Cronin-Golomb, A. (2013). Bisection in Parkinson’s disease: Investigation of contributions of visual field, retinal vision, and scanning patterns to visuospatial function. Behavioral Neuroscience, 127(2), 151163.Google Scholar
Learmonth, G., Benwell, C.S.Y., Thut, G., & Harvey, M. (2017). Age-related reduction of hemispheric lateralisation for spatial attention: An EEG study. NeuroImage, 23(153), 139151.Google Scholar
Learmonth, G., Gallagher, A., Gibson, J., Thut, G., & Harvey, M. (2015). Intra- and inter-task reliability of spatial attention measures in pseudoneglect. PLoS One, 10(9) doi: 10.1371/journal.pone.0138379 Google Scholar
Lee, A.C., Harris, J.P., Atkinson, L., & Fowler, M.S. (2001). Evidence from a line bisection task for visuospatial neglect in left Hemi-Parkinson’s disease. Vision Research, 41, 26772686.Google Scholar
Leplow, B., & Stubinger, C. (1994). Visuospatial functions in patients with spasmotic Torticollis. Perceptual and Motor Skills, 78(3 Pt 2), 13631375.Google Scholar
Marzoli, D., Prete, G., & Tommasi, L. (2014). Perceptual asymmetries and handedness: A neglected link? Frontiers in Psychology, 5, 163.Google Scholar
Müller, J., Kiechl, S., Wenning, G.K., Seppi, K., Willeit, J., Gasperi, A., & Poewe, W. (2002). The prevalence of primary dystonia in the general community. Neurology, 59(6), 941943.Google Scholar
Nutt, J.G., Muenter, M.D., Melton, L.J. III, Aronson, A., & Kurland, L.T. (1988). Epidemiology of dystonia in Rochester, Minnesota. Advances in Neurology Journal, 50, 361365.Google Scholar
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97113.Google Scholar
Perruchoud, D., Murray, M.M., Lefebvre, J., & Ionta, S. (2014). Focal dystonia and the sensory-motor integrative loop for enacting (SMILE). Frontiers in Human Neuroscience, 8, 458.Google Scholar
Picazio, S., Ponzo, V., & Koch, G. (2015). Cerebellar control on prefrontal-motor connectivity during movement inhibition. Cerebellum, 15(6), 680687.Google Scholar
Pierce, C.A., Jewell, G., & Mennemeier, M. (2003). Are psychophysical functions derived from line bisection reliable? Journal of the International Neuropsychological Society, 9(1), 7278.Google Scholar
Premi, E., Diano, M., Gazzina, S., Cauda, F., Gualeni, V., Tinazzi, M., & Borroni, B. (2016). Functional connectivity networks in asymptomatic and symptomatic DYT1 carriers. Movement Disorders, 31(11), 17391743.Google Scholar
Proctor, F., Riklan, M., Cooper, I.S., & Teuber, H.L. (1964). Judgment of visual and postural vertical by parkinsonian patients. Neurology, 14, 287293.Google Scholar
Prudente, C.N., Hess, E.J., & Jinnah, H.A. (2014). Dystonia as a network disorder: What is the role of the cerebellum? Neuroscience, 260, 2335.Google Scholar
Quartarone, A., & Hallett, M. (2013). Emerging concepts in the physiological basis of dystonia. Movement Disorders, 28(7), 958967.Google Scholar
Quartarone, A., Rizzo, V., Terranova, C., Milardi, D., Bruschetta, D., Ghilardi, M.F., & Girlanda, P. (2014). Sensory abnormalities in focal hand dystonia and non-invasive brain stimulation. Frontiers in Human Neuroscience, 8, 956.Google Scholar
Rao, N.P., Arasappa, R., Reddy, N.N., Venkatasubramanian, G., & Reddy, Y.C.J. (2015). Lateralisation abnormalities in obsessive-compulsive disorder: A line bisection study. Acta Neuropsychiatrica, 27(4), 242247.Google Scholar
Ricci, R., Calhoun, J., & Chatterjee, A. (2000). Orientation bias in unilateral neglect: Representational contributions. Cortex, 36(5), 671677.CrossRefGoogle ScholarPubMed
Ricci, R., & Chatterjee, A. (2001). Context and crossover in unilateral neglect. Neuropsychologia, 39(11), 11381143.Google Scholar
Ricci, R., Mazzeo, G., Celentano, B., Nobili, M., & Salatino, A. (2015). Repetitive transcranial magnetic stimulation of the posterior parietal cortex for the treatment of focal dystonia. Proceedings of XXIII National Congress of the Italian Society of Psychophysiology. Neuropsychological Trends - ISSN:1970-321X.Google Scholar
Ricci, R., Salatino, A., Li, X., Funk, A.P., Logan, S.L., Mu, Q., & George, M.S. (2012). Imaging the neural mechanisms of TMS neglect-like bias in healthy volunteers with the interleaved TMS/fMRI technique: Preliminary evidence. Frontiers in Human Neuroscience, 6, 326.Google Scholar
Ricci, R., Salatino, A., Siebner, H., Mazzeo, G., & Nobili, M. (2014). Normalizing biased spatial attention with parietal rTMS in a patient with focal hand dystonia. Brain Stimulation, 7(6), 912.Google Scholar
Roth, H.L., Lora, A.N., & Heilman, K.M. (2002). Effects of monocular viewing and eye dominance on spatial attention. Brain, 125(Pt 9), 20232035.Google Scholar
Salatino, A., Poncini, M., George, M.S., & Ricci, R. (2014). Hunting for right and left parietal hot spots using single-pulse TMS: Modulation of visuospatial perception during line bisection judgment in the healthy brain. Frontiers in Psychology, 5, 1238.Google Scholar
Savazzi, S., Posteraro, L., Veronesi, G., & Mancini, F. (2007). Rightward and leftward bisection biases in spatial neglect: Two sides of the same coin? Brain, 130(Pt 8), 20702084.Google Scholar
Schenkenberg, T., Bradford, D.C., & Ajax, E.T. (1980). Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurology, 30(5), 509517.Google Scholar
Schindler, I., & Kerkhoff, G. (1997). Head and trunk orientation modulate visual neglect. Neuroreport, 8(12), 26812685.Google Scholar
Schneider, C.W., & Bartley, H. (1962). A study of the effects of mechanically induced tension of the neck muscles on the perception of verticality. Journal of Psychology, 54, 245248.CrossRefGoogle Scholar
Schneider, S., Feifel, E., Ott, D., Schumacher, M., Lücking, C.H., & Deuschl, G. (1994). Prolonged MRI T2 times of the lentiform nucleus in idiopathic spasmodic Torticollis. Neurology, 44(5), 846850.Google Scholar
Starkstein, S., Leiguarda, R., Gershanik, O., & Berthier, M. (1987). Neuropsychological disturbances in hemiparkinson’s disease. Neurology, 37, 17621764.Google Scholar
Thiebaut de Schotten, M., Dell’Acqua, F., Forkel, S.J., Simmons, A., Vergani, F., Murphy, D.G.M., &Catani, M. (2011). A lateralized brain network for visuospatial attention. Nature Neuroscience, 14, 12451246.Google Scholar
Tinazzi, M., Fiorio, M., Fiaschi, A., Rothwell, J.C., & Bhatia, K.P. (2009). Sensory functions in dystonia: Insights from behavioral studies. Movement Disorders, 24(10), 14271436.Google Scholar
Tsui, J.K.C., Eisen, A., Stoessl, A.J., Calne, S., & Calne, D.B. (1986). Double-blind study of botulinum toxin in spasmodic Torticollis. The Lancet, 2, 245.Google Scholar
Wilkins, R.H., & Rengachary, S.S. Spasmodic torticollis. (1996). Neurosurgery (2nd ed., pp 41594161). New York: McGraw-Hill.Google Scholar
Yang, E., Blake, R., & McDonald, J.E. II. (2010). A new interocular suppression technique for measuring sensory eye dominance. Visual Psychophysics and Physiological Optics, 51, 588593.Google Scholar