Freezing beyond gait in Parkinson's disease: A review of current neurobehavioral evidence

Neuroscience and Biobehavioral Reviews

Volumn 43, Issue , 2014, Pages 213-227

  Vercruysse, S ^a   Gilat, M ^b   Shine, J M ^b   Heremans, E ^a   Lewis, S ^b   Nieuwboer, A ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Basal ganglia; Festination; Freezing; Freezing of gait; Lower limb; Motor block; Neuroimaging; Parkinson's disease; Speech; Upper limb

Indexed keywords

ARM MOVEMENT; BASAL GANGLION; CLINICAL FEATURE; CONCEPTUAL FRAMEWORK; DISEASE ASSOCIATION; FREEZING OF GAIT; GAIT DISORDER; HUMAN; LEG MOVEMENT; MOTOR CONTROL; NEUROIMAGING; NEUROPATHOLOGY; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SPEECH DISORDER; COMPLICATION; GAIT DISORDERS, NEUROLOGIC; PATHOPHYSIOLOGY;

GAIT DISORDERS, NEUROLOGIC; HUMANS; PARKINSON DISEASE;

EID: 84899804782     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2014.04.010     Document Type: Review

References (76)

1. Abe K., Asai Y., Matsuo Y., Nomura T., Sato S., Inoue S., Mizukura I., Sakoda S. Classifying lower limb dynamics in Parkinson's disease. Brain Res. Bull. 2003, 61:219-226.
2. Ackermann H., Gröne B.F., Hoch G., Schönle P.W. Speech freezing in Parkinson's disease: a kinematic analysis of orofacial movements by means of electromagnetic articulography. Folia Phoniatr. (Basel) 1993, 45:84-89.
3. Almeida Q.J., Wishart L.R., Lee T.D. Bimanual coordination deficits with Parkinson's disease: the influence of movement speed and external cueing. Mov. Disord. 2002, 17:30-37.
4. Almeida Q.J., Wishart L.R., Lee T.D. Disruptive influences of a cued voluntary shift on coordinated movement in Parkinson's disease. Neuropsychologia 2003, 41:442-452.
5. Barbe M.T., Amarell M., Snijders A.H., Florin E., Quatuor E.L., Schönau E., Fink G.R., Bloem B.R., Timmermann L. Gait and upper limb variability in Parkinson's disease patients with and without freezing of gait. J. Neurol. 2014, 261:330-342.
6. Bartels A.L., de Jong B.M., Giladi N., Schaafsma J.D., Maguire R.P., Veenma L., Pruim J., Balash Y., Youdim M.B., Leenders K.L. Striatal dopa and glucose metabolisms in PD patients with freezing of gait. Mov. Disord. 2006, 21:13326-13332.
7. Bartels A.L., Leenders K.L. Brain imaging in patients with freezing of gait. Mov. Disord. 2008, 23:S461-S467.
8. Bloem B.R., Hausdorff J.M., Visser J.E., Giladi N. Falls and freezing of gait in Parkinson's disease: a review of two interconnected, episodic phenomena. Mov. Disord. 2004, 19:871-884.
9. Bronfeld M., Bar-Gad I. Loss of specificity in Basal Ganglia related movement disorders. Front. Syst. Neurosci. 2011, 38:1-13.
10. Bronte-Stewart H.M., Ding L., Alexander C., Zhou Y., Moore G.P. Quantitative digitography (QDG): a sensitive measure of digital motor control in idiopathic Parkinson's disease. Mov. Disord. 2000, 15:36-47.
11. Cantiniaux S., Vaugoyeau M., Robert D., Horrelou-Pitek C., Mancini J., Witjas T., Azulay J.P. Comparative analysis of gait and speech in Parkinson's disease: hypokinetic or dysrhythmic disorders?. J. Neurol. Neurosurg. Psychiatry 2010, 81:177-184.
12. Chee R., Murphy A., Danoudis M., Georgiou-Karistianis N., Iansek R. Gait freezing in Parkinson's disease and the stride length sequence effect interaction. Brain 2009, 132:2151-2160.
13. Espay A.J., Fasano A., van Nuenen B.F., Payne M.M., Snijders A.H., Bloem B.R. On state freezing of gait in Parkinson disease: a paradoxical levodopa-induced complication. Neurology 2012, 78:454-457.
14. Giladi N., Horak F.B., Hausdorff J.M. Classification of gait disturbances. Distinguishing between continuous and episodic changes. Mov. Disord. 2013, 28:1469-1473.
15. Giladi N., McDermott M.P., Fahn S., Przedborski S., Jankovic J., Stern M., Tanner C., Parkinson Study Group Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 2001, 56:1712-1721.
16. Giladi N., McMahon D., Przedborski S., Flaster E., Guillory S., Kostic V., Fahn S. Motor blocks in Parkinson's disease. Neurology 1992, 42:333-339.
17. Gilat M., Shine J.M., Bolitho S.J., Matar E., Kamsma Y.P., Naismith S.L., Lewis S.J. Variability of stepping during a virtual reality paradigm in Parkinson's disease patients with and without freezing of gait. PLoS ONE 2013, 8:e66718.
18. Hausdorff J.M., Balash Y., Giladi N. Time series analysis of leg movements during freezing of gait in Parkinson's disease: akinesia, rhyme or reason?. Physica A 2003, 321:565-570.
19. Handojoseno A.M., Shine J.M., Nguyen T.N., Tran Y., Lewis S.J., Nguyen H.T. Using EEG spatial correlation, cross frequency energy, and wavelet coefficients for the prediction of Freezing of Gait in Parkinson's Disease patients. Conf. Proc. I.E.E.E. Eng. Med. Biol. Soc. 2013 2013, 4263-4266.
20. Helmich R.C., Derikx L.C., Bakker M., Scheeringa R., Bloem B.R., Toni I. Spatial remapping of cortico-striatal connectivity in Parkinson's disease. Cereb. Cortex 2010, 20:1175-1186.
21. Heremans E., Nieuwboer A., Spildooren J., Vandenbossche J., Deroost N., Soetens E., Kerckhofs E., Vercruysse S. Cognitive aspects of freezing of gait in Parkinson's disease: a challenge for rehabilitation. J. Neural Transm. 2013, 120:543-557.
22. Heremans E., Nieuwboer A., Vercruysse S. Freezing of gait in Parkinson's disease: where are we now?. Curr. Neurol. Neurosci. Rep. 2013, 13:350.
23. Iansek R., Huxham F., McGinley J. The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait?. Mov. Disord. 2006, 21:1419-1424.
24. Jacobs J.V., Nutt J.G., Carlson-Kuhta P., Stephens M., Horak F.B. Knee trembling during freezing of gait represents multiple anticipatory postural adjustments. Exp. Neurol. 2009, 215:334-341.
25. Jankovic J. Parkinson's disease: clinical features and diagnosis. J. Neurol. Neurosurg. Psychiatry 2008, 79:368-376.
26. Jones C.R., Claassen D.O., Yu M., Spies J.R., Malone T., Dirnberger G., Jahanshahi M., Kubovy M. Modeling accuracy and variability of motor timing in treated and untreated Parkinson's disease and healthy controls. Front. Integr. Neurosci. 2011, 5:81.
27. Kelly V.E., Eusterbrock A.J., Shumway-Cook A. A review of dual-task walking deficits in people with Parkinson's disease: motor and cognitive contributions, mechanisms, and clinical implications. Parkinsons Dis. 2012, 2012:918719.
28. Kerr G.K., Worringham C.J., Cole M.H., Lacherez P.F., Wood J.M., Silburn P.A. Predictors of future falls in Parkinson disease. Neurology 2010, 75:116-124.
29. Kostic V.S., Agosta F., Pievani M., Stefanova E., Jecmenica-Lukic M., Scarale A., Spica V., Filippi M. Pattern of brain tissue loss associated with freezing of gait in Parkinson disease. Neurology 2012, 78:409-416.
30. Lewis S.J., Barker R.A. A pathophysiological model of freezing of gait in Parkinson's disease. Parkinsonism Relat. Disord. 2009, 15:333-338.
31. Lim I., van Wegen E., de Goede C., Deutekom M., Nieuwboer A., Willems A., Jones D., Rochester L., Kwakkel G. Effects of external rhythmical cueing on gait in patients with Parkinson's disease: a systematic review. Clin. Rehabil. 2005, 19:695-713.
32. Macht M., Kaussner Y., Möller J.C., Stiasny-Kolster K., Eggert K.M., Krüger H.P., Ellgring H. Predictors of freezing in Parkinson's disease: a survey of 6,620 patients. Mov. Disord. 2007, 22:953-956.
33. Matsui H., Udaka F., Miyoshi T., Hara N., Tamaura A., Oda M., Kubori T., Nishinaka K., Kameyama M. Three-dimensional stereotactic surface projection study of freezing of gait and brain perfusion image in Parkinson's disease. Mov. Disord. 2005, 20:1272-1277.
34. Matar E., Shine J.M., Naismith S.L., Lewis S.J. Using virtual reality to explore the role of conflict resolution and environmental salience in Freezing of Gait in Parkinson's disease. Parkinsonism Relat. Disord. 2013, pii:S1353-8020(13)00220-4.10.1016.
35. Moore O., Peretz C., Giladi N. Freezing of gait affects quality of life of people with Parkinson's disease beyond its relationship with mobility and gait. Mov. Disord. 2007, 15:2192-2195.
36. Moreau C., Ozsancak C., Blatt J.L., Derambure P., Destee A., Defebvre L. Oral festination in Parkinson's disease: biomechanical analysis and correlation with festination and freezing of gait. Mov. Disord. 2007, 22:1503-1506.
37. Nagasaki H., Itoh H., Hashizume K., Furuna T., Maruyama H., Kinugasa T. Walking patterns and finger rhythm of older adults. Percept. Mot. Skills 1996, 82:435-447.
38. Naismith S.L., Lewis S.J. A novel paradigm for modelling freezing of gait in Parkinson's disease. J. Clin. Neurosci. 2010, 17:984-987.
39. Nantel J., de Solages C., Bronte-Stewart H. Repetitive stepping in place identifies and measures freezing episodes in subjects with Parkinson's disease. Gait Posture 2011, 34:329-333.
40. Nantel J., McDonald J.C., Tan S., Bronte-Stewart H. Deficits in visuospatial processing contribute to quantitative measures of freezing of gait in Parkinson's disease. Neuroscience 2012, 221:151-156.
41. Nieuwboer A., Dom R., De Weerdt W., Desloovere K., Fieuws S., Broens-Kaucsik E. Abnormalities of the spatiotemporal characteristics of gait at the onset of freezing in Parkinson's disease. Mov. Disord. 2001, 16:1066-1075.
42. Nieuwboer A., Dom R., De Weerdt W., Desloovere K., Janssens L., Stijn V. Electromyographic profiles of gait prior to onset of freezing episodes in patients with Parkinson's disease. Brain 2004, 127:1650-1660.
43. Nieuwboer A., Fabienne C., Willems A., Desloovere K. Does freezing in Parkinson's disease change limb coordination? A kinematic analysis. J. Neurol. 2007, 254:1268-1277.
44. Nieuwboer A., Giladi N. Characterizing freezing of gait in Parkinson's disease. Models of an episodic phenomenon. Mov. Disord. 2013, 28:1509-1519.
45. Nieuwboer A., Vercruysse S., Feys P., Levin O., Spildooren J., Swinnen S. Upper limb movement interruptions are correlated to freezing of gait in Parkinson's disease. Eur. J. Neurosci. 2009, 29:1422-1430.
46. Nutt J.G., Bloem B.R., Giladi N., Hallett M., Horak F.B., Nieuwboer A. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol. 2011, 10:734-744.
47. Obeso J.A., Rodriguez-Oroz M.C., Benitez-Temino B., Blesa F.J., Guridi J., Marin C., Rodriguez M. Functional organization of the basal ganglia: therapeutic implications for Parkinson's disease. Mov. Disord. 2008, 23:S548-S559.
48. Park H.K., Yoo J.Y., Kwon M., Lee J.H., Lee S.J., Kim S.R., Kim M.J., Lee M.C., Lee S.M., Chung S.J. Gait freezing and speech disturbance in Parkinson's disease. Neurol. Sci. 2014, 35:357-363.
49. Plotnik M., Giladi N., Balash Y., Peretz C., Hausdorff J.M. Is freezing of gait in Parkinson's disease related to asymmetric motor function?. Ann. Neurol. 2005, 57:656-663.
50. Plotnik M., Giladi N., Hausdorff J.M. Bilateral coordination of walking and freezing of gait in Parkinson's disease. Eur. J. Neurosci. 2008, 27:1999-2006.
51. Plotnik M., Giladi N., Hausdorff J.M. Is freezing of gait in Parkinson's disease a result of multiple gait impairments? Implications for treatment. Parkinsons Dis. 2012, 2012:1-8.
52. Popovic M.B., Dzoljic E., Kostic V. A method to assess hand motor blocks in Parkinson's disease with digitizing tablet. Tohoku J. Exp. Med. 2008, 216:317-324.
53. Redgrave P., Rodriguez M., Smith Y., Rodriguez-Oroz M.C., Lehericy S., Bergman H., Agid Y., DeLong M.R., Obeso J.A. Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease. Nat. Rev. Neurosci. 2010, 11:760-772.
54. Sauermann S., Standhardt H., Gerschlager W., Lanmüller H., Alesch F. Kinematic evaluation in Parkinson's disease using a hand-held position transducer and computerized signal analysis. Acta Neurochir. (Wien) 2005, 147:939-945.
55. Schaafsma J.D., Balash Y., Gurevich T., Bartels A.L., Hausdorff J.M., Giladi N. Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson's disease. Eur. J. Neurol. 2003, 10:391-398.
56. Schweder P.M., Hansen P.C., Green A.L., Quaghebeur G., Stein J., Aziz T.Z. Connectivity of the pedunculopontine nucleus in parkinsonian freezing of gait. Neuroreport 2010, 21:914-916.
57. Shine J.M., Matar E., Ward P.B., Bolitho S.J., Gilat M., Pearson M., Naismith S.L., Lewis S.J. Exploring the cortical and subcortical functional magnetic resonance imaging changes associated with freezing in Parkinson's disease. Brain 2013, 136:1204-1215.
58. Shine J.M., Matar E., Ward P.B., Bolitho S.J., Pearson M., Naismith S.L., Lewis S.J. Differential neural activation patterns in patients with Parkinson's disease and freezing of gait in response to concurrent cognitive and motor load. PLoS ONE 2013, 8:e52602.
59. Shine J.M., Matar E., Ward P.B., Frank M.J., Moustafa A.A., Pearson M., Naismith S.L., Lewis S.J. Freezing of gait in Parkinson's disease is associated with functional decoupling between the cognitive control network and the basal ganglia. Brain 2013, 136:3671-3681.
60. Shine J.M., Moustafa A.A., Matar E., Frank M.J., Lewis S.J. The role of frontostriatal impairment in freezing of gait in Parkinson's disease. Front. Syst. Neurosci. 2013, 7:61.
61. Shine J.M., Matar E., Bolitho S.J., Dilda V., Morris T.R., Naismith S.L., Moore S.T., Lewis S.J. Modeling freezing of gait in Parkinson's disease with a virtual reality paradigm. Gait Posture 2013, 38:104-108.
62. Snijders A.H., Bloem B.R. Cycling for freezing of gait. N. Engl. J. Med. 2010, 362:e46.
63. Snijders A.H., Leunissen I., Bakker M., Overeem S., Helmich R.C., Bloem B.R., Toni I. Gait-related cerebral alterations in patients with Parkinson's disease with freezing of gait. Brain 2011, 134:59-72.
64. Stegemöller E.L., Simuni T., MacKinnon C. Effect of movement frequency on repetitive finger movements in patients with Parkinson's disease. Mov. Disord. 2009, 24:1162-1169.
65. Stegemöller E.L., Zadikoff C., Rosenow J.M., Mackinnon C.D. Deep brain stimulation improves movement amplitude but not hastening of repetitive finger movements. Neurosci. Lett. 2013, 552:135-139.
66. Tessitore A., Amboni M., Cirillo G., Corbo D., Picillo M., Russo A., Vitale C., Santangelo G., Erro R., Cirillo M., Esposito F., Barone P., Tedeschi G. Regional gray matter atrophy in patients with parkinson disease and freezing of gait. AJNR Am. J. Neuroradiol. 2012, 33:1804-1809.
67. Tessitore A., Amboni M., Esposito F., Russo A., Picillo M., Marcuccio L., Pellecchia M.T., Vitale C., Cirillo M., Tedeschi G., Barone P. Resting-state brain connectivity in patients with Parkinson's disease and freezing of gait. Parkinsonism Relat. Disord. 2012, 18:781-787.
68. Vandenbossche J., Deroost N., Soetens E., Coomans D., Spildooren J., Vercruysse S., Nieuwboer A., Kerckhofs E. Freezing of gait in Parkinson's disease: disturbances in automaticity and control. Front. Hum. Neurosci. 2012, 6:356.
69. Vercruysse S., Spildooren J., Heremans E., Vandenbossche J., Levin O., Wenderoth N., Swinnen S.P., Janssens L., Vandenberghe W., Nieuwboer A. Freezing in Parkinson's disease: a spatiotemporal motor disorder beyond gait. Mov. Disord. 2012, 27:254-263.
70. Vercruysse S., Devos H., Munks L., Spildooren J., Vandenbossche J., Vandenberghe W., Nieuwboer A., Heremans E. Explaining freezing of gait in Parkinson's disease: motor and cognitive determinants. Mov. Disord. 2012, 27:1644-1651.
71. Vercruysse S., Spildooren J., Heremans E., Vandenbossche J., Wenderoth N., Swinnen S.P., Vandenberghe W., Nieuwboer A. Abnormalities and cue dependence of rhythmical upper-limb movements in Parkinson patients with freezing of gait. Neurorehabil. Neural Repair 2012, 26:636-645.
72. Vercruysse S., Spildooren J., Heremans E., Wenderoth N., Swinnen S.P., Vandenberghe W., Nieuwboer A. The neural correlates of upper limb motor blocks in Parkinson's disease and their relation to freezing of gait. Cereb. Cortex 2013, (in press). 10.1093/cercor/bht170.
73. Williams A.J., Peterson D.S., Ionno M., Pickett K.A., Earhart G.M. Upper extremity freezing and dyscoordination in Parkinson's disease: effects of amplitude and cadence manipulations. Parkinsons. Dis. 2013, 2013:595378.
74. Yahalom G., Simon E.S., Thorne R., Peretz C., Giladi N. Hand rhythmic tapping and timing in Parkinson's disease. Parkinsonism Relat. Disord. 2004, 10:143-148.
75. Ziv I., Avraham M., Dabby R., Zoldan J., Djaldetti R., Melamed E. Early-occurrence of manual motor blocks in Parkinson's disease: a quantitative assessment. Acta Neurol. Scand. 1999, 99:106-111.
76. Zwergal A., Linn J., Xiong G., Brandt T., Strupp M., Jahn K. Aging of human supraspinal locomotor and postural control in fMRI. Neurobiol. Aging 2012, 33:1073-1084.