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Published in: Current Neurology and Neuroscience Reports 6/2013

01-06-2013 | Movement Disorders (SA Factor, Section Editor)

Freezing of Gait in Parkinson’s Disease: Where Are We Now?

Authors: Elke Heremans, Alice Nieuwboer, Sarah Vercruysse

Published in: Current Neurology and Neuroscience Reports | Issue 6/2013

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Abstract

Freezing of gait (FOG) is defined as a brief, episodic absence or marked reduction of forward progression of the feet despite the intention to walk. It is one of the most debilitating motor symptoms in patients with Parkinson’s disease (PD) as it may lead to falls and a loss of independence. The pathophysiology of FOG seems to differ from the cardinal features of PD and is still largely unknown. In the present paper, we review the studies that were performed since 2011 on methods to provoke and assess FOG and discuss new insights into behavioral and neural mechanisms underlying this clinical phenomenon. We conclude that most of the work reviewed confirms that gait pattern generation disturbances are central to FOG. The finding that FOG reflects a combined motor and cognitive de-automatization deficit, which may not be sufficiently offset by executive control, probably acts as parallel mechanism.
Literature
1.
go back to reference •• Nutt JG, Bloem BR, Giladi N, et al. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol. 2011;10:734–44. This paper reviews the knowledge with regard to freezing of gait up to 2011 and formulates 5 hypotheses on its origins.PubMedCrossRef •• Nutt JG, Bloem BR, Giladi N, et al. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol. 2011;10:734–44. This paper reviews the knowledge with regard to freezing of gait up to 2011 and formulates 5 hypotheses on its origins.PubMedCrossRef
2.
go back to reference Macht M, Kaussner Y, Möller JC, et al. Predictors of freezing in Parkinson’s disease: a survey of 6620 patients. Mov Disord. 2007;22:753–6.CrossRef Macht M, Kaussner Y, Möller JC, et al. Predictors of freezing in Parkinson’s disease: a survey of 6620 patients. Mov Disord. 2007;22:753–6.CrossRef
3.
go back to reference Lopez IC, Ruiz PJ, Del Pozo SV, et al. Motor complications in Parkinson’s disease: a 10 year follow-up study. Mov Disord. 2010;25:2735–9.PubMedCrossRef Lopez IC, Ruiz PJ, Del Pozo SV, et al. Motor complications in Parkinson’s disease: a 10 year follow-up study. Mov Disord. 2010;25:2735–9.PubMedCrossRef
4.
go back to reference Giladi N, McDermott MP, Fahn S, et al. Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology. 2001;56:1712–21.PubMedCrossRef Giladi N, McDermott MP, Fahn S, et al. Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology. 2001;56:1712–21.PubMedCrossRef
5.
go back to reference Rahman S, Griffin HJ, Quinn NP, et al. Quality of life in Parkinson’s disease: the relative importance of the symptoms. Mov Disord. 2008;23:1428–34.PubMedCrossRef Rahman S, Griffin HJ, Quinn NP, et al. Quality of life in Parkinson’s disease: the relative importance of the symptoms. Mov Disord. 2008;23:1428–34.PubMedCrossRef
6.
go back to reference Tan D, Danoudis M, McGinley J, et al. Relationships between motor aspects of gait impairments and activity limitations in people with Parkinson’s disease: a systematic review. Parkinsonism Relat Disord. 2012;18:117–24.PubMedCrossRef Tan D, Danoudis M, McGinley J, et al. Relationships between motor aspects of gait impairments and activity limitations in people with Parkinson’s disease: a systematic review. Parkinsonism Relat Disord. 2012;18:117–24.PubMedCrossRef
7.
go back to reference Bartels AL, Balash Y, Gurevich T, et al. Relationship between freezing of gait (FOG) and other features of Parkinson’s: FOG is not correlated with bradykinesia. J Clin Neurosci. 2003;10:584–8.PubMedCrossRef Bartels AL, Balash Y, Gurevich T, et al. Relationship between freezing of gait (FOG) and other features of Parkinson’s: FOG is not correlated with bradykinesia. J Clin Neurosci. 2003;10:584–8.PubMedCrossRef
8.
go back to reference Hely MA, Reid WG, Adena MA, et al. The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord. 2008;23:837–44.PubMedCrossRef Hely MA, Reid WG, Adena MA, et al. The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord. 2008;23:837–44.PubMedCrossRef
9.
go back to reference Ferraye MU, Debû B, Fraix V, et al. Effects of subthalamic nucleus stimulation and levodopa on freezing of gait in Parkinson disease. Neurology. 2008;70:1431–7.PubMedCrossRef Ferraye MU, Debû B, Fraix V, et al. Effects of subthalamic nucleus stimulation and levodopa on freezing of gait in Parkinson disease. Neurology. 2008;70:1431–7.PubMedCrossRef
10.
go back to reference Willems AM, Nieuwboer A, Chavret F, et al. The use of rhythmic auditory cues to influence gait in patients with Parkinson’s disease, the differential effect for freezers and nonfreezers, an explorative study. Disabil Rehabil. 2006;28:721–8.PubMedCrossRef Willems AM, Nieuwboer A, Chavret F, et al. The use of rhythmic auditory cues to influence gait in patients with Parkinson’s disease, the differential effect for freezers and nonfreezers, an explorative study. Disabil Rehabil. 2006;28:721–8.PubMedCrossRef
11.
go back to reference Giladi N, Tal J, Azulay T, et al. Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov Disord. 2009;24:655–61.PubMedCrossRef Giladi N, Tal J, Azulay T, et al. Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov Disord. 2009;24:655–61.PubMedCrossRef
12.
go back to reference Nieuwboer A, Rochester L, Herman T, et al. Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture. 2009;30:459–63.PubMedCrossRef Nieuwboer A, Rochester L, Herman T, et al. Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture. 2009;30:459–63.PubMedCrossRef
13.
go back to reference Snijders AH, Haaxma CA, Hagen YJ, et al. Freezer or nonfreezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord. 2012;18:149–54.PubMedCrossRef Snijders AH, Haaxma CA, Hagen YJ, et al. Freezer or nonfreezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord. 2012;18:149–54.PubMedCrossRef
14.
go back to reference 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;34:329–33.PubMedCrossRef 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;34:329–33.PubMedCrossRef
15.
go back to reference Morris TR, Cho C, Dilda V, et al. A comparison of clinical and objective measures of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:572–7.PubMedCrossRef Morris TR, Cho C, Dilda V, et al. A comparison of clinical and objective measures of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:572–7.PubMedCrossRef
16.
go back to reference Ziegler K, Schroeteler F, Ceballos-Baumann AO, et al. A new rating instrument to assess festination and freezing of gait in Parkinsonian patients. Mov Disord. 2010;25:1012–8.PubMedCrossRef Ziegler K, Schroeteler F, Ceballos-Baumann AO, et al. A new rating instrument to assess festination and freezing of gait in Parkinsonian patients. Mov Disord. 2010;25:1012–8.PubMedCrossRef
17.
go back to reference Crémers J, Phan Ba R, Delvaux V, et al. Construction and validation of the Dynamic Parkinson Gait Scale (DYPAGS). Parkinsonism Relat Disord. 2012;18:759–64.PubMedCrossRef Crémers J, Phan Ba R, Delvaux V, et al. Construction and validation of the Dynamic Parkinson Gait Scale (DYPAGS). Parkinsonism Relat Disord. 2012;18:759–64.PubMedCrossRef
18.
go back to reference Moore ST, MacDougall HG, Ondo WG. Ambulatory monitoring of freezing of gait in Parkinson’s disease. J Neurosci Methods. 2008;167:340–8.PubMedCrossRef Moore ST, MacDougall HG, Ondo WG. Ambulatory monitoring of freezing of gait in Parkinson’s disease. J Neurosci Methods. 2008;167:340–8.PubMedCrossRef
19.
go back to reference Delval A, Snijders A, Weerdesteyn V, et al. Objective detection of subtle freezing of gait episodes in Parkinson’s disease. Mov Disord. 2010;11:1684–93.CrossRef Delval A, Snijders A, Weerdesteyn V, et al. Objective detection of subtle freezing of gait episodes in Parkinson’s disease. Mov Disord. 2010;11:1684–93.CrossRef
20.
go back to reference Frenkel-Toledo S, Giladi N, Peretz C, et al. Treadmill walking as an external pacemaker to improve gait rhythm and stability in Parkinson’s disease. Mov Disord. 2005;20:1109–14.PubMedCrossRef Frenkel-Toledo S, Giladi N, Peretz C, et al. Treadmill walking as an external pacemaker to improve gait rhythm and stability in Parkinson’s disease. Mov Disord. 2005;20:1109–14.PubMedCrossRef
21.
go back to reference Mancini M, Priest KC, Nutt JG, et al. Quantifying freezing of gait in Parkinson’s disease during the instrumented timed up and go test. Conf Proc IEEE Eng Med Biol Soc. 2012;2012:1198–201.PubMed Mancini M, Priest KC, Nutt JG, et al. Quantifying freezing of gait in Parkinson’s disease during the instrumented timed up and go test. Conf Proc IEEE Eng Med Biol Soc. 2012;2012:1198–201.PubMed
22.
go back to reference Naismith SL, Lewis SJ. A novel paradigm for modelling freezing of gait in Parkinson’s disease. J Clin Neurosci. 2010;17:984–7.PubMedCrossRef Naismith SL, Lewis SJ. A novel paradigm for modelling freezing of gait in Parkinson’s disease. J Clin Neurosci. 2010;17:984–7.PubMedCrossRef
23.
go back to reference Snijders AH, Bloem BR. Images in clinical medicine. Cycling for freezing of gait. N Engl J Med. 2010;362:e46.PubMedCrossRef Snijders AH, Bloem BR. Images in clinical medicine. Cycling for freezing of gait. N Engl J Med. 2010;362:e46.PubMedCrossRef
24.
go back to reference Shine JM, Matar E, Ward PB, et al. 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.PubMedCrossRef Shine JM, Matar E, Ward PB, et al. 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.PubMedCrossRef
25.
go back to reference Snijders AH, Leunissen I, Bakker M, et al. Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain. 2011;134:59–72.PubMedCrossRef Snijders AH, Leunissen I, Bakker M, et al. Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain. 2011;134:59–72.PubMedCrossRef
26.
go back to reference Cisek P, Kalaska JF. Neural correlates of mental rehearsal in dorsal premotor cortex. Nature. 2004;431:993–6.PubMedCrossRef Cisek P, Kalaska JF. Neural correlates of mental rehearsal in dorsal premotor cortex. Nature. 2004;431:993–6.PubMedCrossRef
27.
go back to reference Miller KJ, Schalk G, Fetz EE, et al. Cortical activity during motor execution, motor imagery, and imagery-based online feedback. Proc Natl Acad Sci USA. 2010;107:4430–5.PubMedCrossRef Miller KJ, Schalk G, Fetz EE, et al. Cortical activity during motor execution, motor imagery, and imagery-based online feedback. Proc Natl Acad Sci USA. 2010;107:4430–5.PubMedCrossRef
28.
go back to reference Bakker M, de Lange FP, Helmich RC, et al. Cerebral correlates of motor imagery of normal and precision gait. Neuroimage. 2008;41:998–1010.PubMedCrossRef Bakker M, de Lange FP, Helmich RC, et al. Cerebral correlates of motor imagery of normal and precision gait. Neuroimage. 2008;41:998–1010.PubMedCrossRef
29.
go back to reference Jahn K, Deutschlander A, Stephan T, et al. Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. Neuroimage. 2004;22:1722–31.PubMedCrossRef Jahn K, Deutschlander A, Stephan T, et al. Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. Neuroimage. 2004;22:1722–31.PubMedCrossRef
30.
go back to reference la Fougere C, Zwergal A, Rominger A, et al. Real vs imagined locomotion: a [(18)F]-FDG PET-fMRI comparison. Neuroimage. 2010;50:1589–98.PubMedCrossRef la Fougere C, Zwergal A, Rominger A, et al. Real vs imagined locomotion: a [(18)F]-FDG PET-fMRI comparison. Neuroimage. 2010;50:1589–98.PubMedCrossRef
31.
go back to reference Nieuwboer A, Vercruysse S, Feys P, et al. Upper limb movement interruptions are correlated to freezing of gait in Parkinson's disease. Eur J Neurosci. 2009;29:1422–30.PubMedCrossRef Nieuwboer A, Vercruysse S, Feys P, et al. Upper limb movement interruptions are correlated to freezing of gait in Parkinson's disease. Eur J Neurosci. 2009;29:1422–30.PubMedCrossRef
32.
go back to reference Vercruysse S, Spildooren J, Vandenbossche J, et al. Freezing in Parkinson’s disease: a spatiotemporal motor disorder beyond gait. Mov Disord. 2012;27:254–63.PubMedCrossRef Vercruysse S, Spildooren J, Vandenbossche J, et al. Freezing in Parkinson’s disease: a spatiotemporal motor disorder beyond gait. Mov Disord. 2012;27:254–63.PubMedCrossRef
33.
go back to reference Vercruysse S, Spildooren J, Heremans E, et al. The neural basis of upper limb freezing in patients with Parkinson’s disease and freezing of gait. Cereb Cortex. Under review. Vercruysse S, Spildooren J, Heremans E, et al. The neural basis of upper limb freezing in patients with Parkinson’s disease and freezing of gait. Cereb Cortex. Under review.
34.
go back to reference Plotnik M, Hausdorff JM. The role of gait rhythmicity and bilateral coordination of stepping in the pathophysiology of freezing of gait in Parkinson’s disease. Mov Disord. 2008;23:444–50.CrossRef Plotnik M, Hausdorff JM. The role of gait rhythmicity and bilateral coordination of stepping in the pathophysiology of freezing of gait in Parkinson’s disease. Mov Disord. 2008;23:444–50.CrossRef
35.
go back to reference Chee R, Murphy A, Danoudis M, et al. Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain. 2009;132:2151–60.PubMedCrossRef Chee R, Murphy A, Danoudis M, et al. Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain. 2009;132:2151–60.PubMedCrossRef
36.
go back to reference Thevathasan W, Cole MH, Graepel CL, et al. A spatiotemporal analysis of gait freezing and the impact of pedunculopontine nucleus stimulation. Brain. 2012;135:1446–54.PubMedCrossRef Thevathasan W, Cole MH, Graepel CL, et al. A spatiotemporal analysis of gait freezing and the impact of pedunculopontine nucleus stimulation. Brain. 2012;135:1446–54.PubMedCrossRef
37.
go back to reference Nanhoe-Mahabier W, Snijders AH, Delval A, et al. Walking patterns in Parkinson’s disease with and without freezing of gait. Neuroscience. 2011;182:217–24.PubMedCrossRef Nanhoe-Mahabier W, Snijders AH, Delval A, et al. Walking patterns in Parkinson’s disease with and without freezing of gait. Neuroscience. 2011;182:217–24.PubMedCrossRef
38.
go back to reference Cowie D, Limousin P, Peters A, et al. Doorway-provoked freezing of gait in Parkinson's disease. Mov Disord. 2012;27:492–9.PubMedCrossRef Cowie D, Limousin P, Peters A, et al. Doorway-provoked freezing of gait in Parkinson's disease. Mov Disord. 2012;27:492–9.PubMedCrossRef
39.
go back to reference Hausdorff JM, Schaafsma JD, Balash Y, et al. Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res. 2003;149:187–94.PubMed Hausdorff JM, Schaafsma JD, Balash Y, et al. Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res. 2003;149:187–94.PubMed
40.
go back to reference Plotnik M, Giladi N, Balash Y, et al. Is freezing of gait in Parkinson’s disease related to asymmetric motor function? Ann Neurol. 2005;57:656–63.PubMedCrossRef Plotnik M, Giladi N, Balash Y, et al. Is freezing of gait in Parkinson’s disease related to asymmetric motor function? Ann Neurol. 2005;57:656–63.PubMedCrossRef
41.
go back to reference Spildooren J, Vercruysse S, Desloovere K, et al. Freezing of gait in Parkinson’s disease: the impact of dual-tasking and turning. Mov Disord. 2010;25:2563–70.PubMedCrossRef Spildooren J, Vercruysse S, Desloovere K, et al. Freezing of gait in Parkinson’s disease: the impact of dual-tasking and turning. Mov Disord. 2010;25:2563–70.PubMedCrossRef
42.
go back to reference Bhatt H, Pieruccini-Faria F, Almeida QJ. Dynamics of turning sharpness influences freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord. 2013;19(2):181–5. Bhatt H, Pieruccini-Faria F, Almeida QJ. Dynamics of turning sharpness influences freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord. 2013;19(2):181–5.
43.
go back to reference Peterson DS, Plotnik M, Hausdorff JM, et al. Evidence for a relationship between bilateral coordination during complex gait tasks and freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:1022–6.PubMedCrossRef Peterson DS, Plotnik M, Hausdorff JM, et al. Evidence for a relationship between bilateral coordination during complex gait tasks and freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:1022–6.PubMedCrossRef
44.
go back to reference Nanhoe-Mahabier W, Snijders AH, Delval A, et al. Split-belt locomotion in Parkinson’s disease with and without freezing of gait. Neuroscience. 2013;236:110–6. Nanhoe-Mahabier W, Snijders AH, Delval A, et al. Split-belt locomotion in Parkinson’s disease with and without freezing of gait. Neuroscience. 2013;236:110–6.
45.
go back to reference Vercruysse S, Spildooren J, Heremans E, et al. Abnormalities and cue-dependence of rhythmical upper limb movements in Parkinson’s disease patients with freezing of gait. Neurorehabil Neural Repair. 2012;26:636–45.PubMedCrossRef Vercruysse S, Spildooren J, Heremans E, et al. Abnormalities and cue-dependence of rhythmical upper limb movements in Parkinson’s disease patients with freezing of gait. Neurorehabil Neural Repair. 2012;26:636–45.PubMedCrossRef
46.
go back to reference Williams AJ, Peterson DS, Earhart GM. Gait coordination in Parkinson disease: effects of step length and cadence manipulations. Gait Posture. [In press]. Williams AJ, Peterson DS, Earhart GM. Gait coordination in Parkinson disease: effects of step length and cadence manipulations. Gait Posture. [In press].
47.
go back to reference Danoudis M, Iansek R, Simpson P. Freezing of gait in Parkinson’s disease: further insights into pathophysiological mechanisms. Parkinsonism Relat Disord. 2012;18:543–7.PubMedCrossRef Danoudis M, Iansek R, Simpson P. Freezing of gait in Parkinson’s disease: further insights into pathophysiological mechanisms. Parkinsonism Relat Disord. 2012;18:543–7.PubMedCrossRef
48.
go back to reference • Plotnik M, Giladi N, Hausdorff JM. Is freezing of gait in Parkinson’s disease a result of multiple gait impairments? Implications for treatment Parkinsons Dis. 2012;2012:459321. This paper reviews gait impairments associated with freezing of gait and proposes a threshold model for FOG. • Plotnik M, Giladi N, Hausdorff JM. Is freezing of gait in Parkinson’s disease a result of multiple gait impairments? Implications for treatment Parkinsons Dis. 2012;2012:459321. This paper reviews gait impairments associated with freezing of gait and proposes a threshold model for FOG.
49.
go back to reference • Vandenbossche J, Deroost N, Soetens E, et al. Freezing of gait in Parkinson’s disease: disturbances in automaticity and control. Front Hum Neurosci. 2012;6:356. This paper reviews the evidence related to a cognitive de-automatization deficit underlying FOG.PubMed • Vandenbossche J, Deroost N, Soetens E, et al. Freezing of gait in Parkinson’s disease: disturbances in automaticity and control. Front Hum Neurosci. 2012;6:356. This paper reviews the evidence related to a cognitive de-automatization deficit underlying FOG.PubMed
50.
go back to reference Spildooren J, Vercruysse S, Meyns P, et al. Turning and unilateral cueing in Parkinson’s disease patients with and without freezing of gait. Neuroscience. 2012;207:298–306.PubMedCrossRef Spildooren J, Vercruysse S, Meyns P, et al. Turning and unilateral cueing in Parkinson’s disease patients with and without freezing of gait. Neuroscience. 2012;207:298–306.PubMedCrossRef
51.
go back to reference Arias P, Cudeiro J. Effect of rhythmic auditory stimulation on gait in Parkinsonian patients with and without freezing of Gait. PLoS One. 2010;5:e9675.PubMedCrossRef Arias P, Cudeiro J. Effect of rhythmic auditory stimulation on gait in Parkinsonian patients with and without freezing of Gait. PLoS One. 2010;5:e9675.PubMedCrossRef
52.
go back to reference Lee SJ, Yoo JY, Ryu JS, et al. The effects of visual and auditory cues on freezing of gait in patients with Parkinson disease. Am J Phys Med Rehabil. 2012;91:2–11.PubMedCrossRef Lee SJ, Yoo JY, Ryu JS, et al. The effects of visual and auditory cues on freezing of gait in patients with Parkinson disease. Am J Phys Med Rehabil. 2012;91:2–11.PubMedCrossRef
53.
go back to reference Nanhoe-Mahabier W, Delval A, Snijders AH, et al. The possible price of auditory cueing: influence on obstacle avoidance in Parkinson’s disease. Mov Disord. 2012;27:574–8.PubMedCrossRef Nanhoe-Mahabier W, Delval A, Snijders AH, et al. The possible price of auditory cueing: influence on obstacle avoidance in Parkinson’s disease. Mov Disord. 2012;27:574–8.PubMedCrossRef
54.
go back to reference Kerr GK, Worringham CJ, Cole MH. Predictors of future falls in Parkinson’s disease. Neurology. 2010;75:116–24.PubMedCrossRef Kerr GK, Worringham CJ, Cole MH. Predictors of future falls in Parkinson’s disease. Neurology. 2010;75:116–24.PubMedCrossRef
55.
go back to reference Jacobs JV, Nutt JG, Carlson-Kuhta P, et al. Knee trembling during freezing of gait represents multiple anticipatory postural adjustments. Exp Neurol. 2009;215:334–41.PubMedCrossRef Jacobs JV, Nutt JG, Carlson-Kuhta P, et al. Knee trembling during freezing of gait represents multiple anticipatory postural adjustments. Exp Neurol. 2009;215:334–41.PubMedCrossRef
56.
go back to reference Spildooren J, Vercruysse S, Heremans E, et al. Head-pelvis coupling is increased during turning in patients with Parkinson’s disease and freezing of gait. Mov Disord. [In press]. Spildooren J, Vercruysse S, Heremans E, et al. Head-pelvis coupling is increased during turning in patients with Parkinson’s disease and freezing of gait. Mov Disord. [In press].
57.
go back to reference Vercruysse S, Devos H, Munks L, et al. Explaining freezing of gait in Parkinson’s Disease: motor and cognitive determinants. Mov Disord. 2012;27(13):1644–51. Vercruysse S, Devos H, Munks L, et al. Explaining freezing of gait in Parkinson’s Disease: motor and cognitive determinants. Mov Disord. 2012;27(13):1644–51.
58.
go back to reference Factor SA, Steenland NK, Higgins DS. Postural instability/gait disturbance in Parkinson’s disease has distinct subtypes: an exploratory analysis. J Neurol Neurosurg Psychiatry. 2011;82:564–8.PubMedCrossRef Factor SA, Steenland NK, Higgins DS. Postural instability/gait disturbance in Parkinson’s disease has distinct subtypes: an exploratory analysis. J Neurol Neurosurg Psychiatry. 2011;82:564–8.PubMedCrossRef
59.
go back to reference Almeida QJ, Lebold CA. Freezing of gait in Parkinson’s disease: a perceptual cause for motor impairment? J Neurol Neurosurg Psychiatry. 2010;81:513–8.PubMedCrossRef Almeida QJ, Lebold CA. Freezing of gait in Parkinson’s disease: a perceptual cause for motor impairment? J Neurol Neurosurg Psychiatry. 2010;81:513–8.PubMedCrossRef
60.
go back to reference Cohen RG, Chao A, Nutt JG, et al. Freezing of gait is associated with a mismatch between motor imagery and motor execution in narrow doorways, not with failure to judge doorway passability. Neuropsychologia. 2011;49:3981–8.PubMedCrossRef Cohen RG, Chao A, Nutt JG, et al. Freezing of gait is associated with a mismatch between motor imagery and motor execution in narrow doorways, not with failure to judge doorway passability. Neuropsychologia. 2011;49:3981–8.PubMedCrossRef
61.
go back to reference Nantel J, McDonald JC, Tan S, et al. Deficits in visuospatial processing contribute to quantitative measures of freezing of gait in Parkinson’s disease. Neuroscience. 2012;221:151–6.PubMedCrossRef Nantel J, McDonald JC, Tan S, et al. Deficits in visuospatial processing contribute to quantitative measures of freezing of gait in Parkinson’s disease. Neuroscience. 2012;221:151–6.PubMedCrossRef
62.
go back to reference Lord S, Archibald N, Mosimann U, et al. Dorsal rather than ventral visual pathways discriminate freezing status in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:1094–6.PubMedCrossRef Lord S, Archibald N, Mosimann U, et al. Dorsal rather than ventral visual pathways discriminate freezing status in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:1094–6.PubMedCrossRef
63.
go back to reference • Heremans E, Nieuwboer A, Spildooren J, et al. Cognitive aspects of freezing of gait in Parkinson’s disease: a challenge for rehabilitation. J Neural Transm. 2013;120(4):543–57. This paper reviews the evidence on cognitive disturbance related to FOG. • Heremans E, Nieuwboer A, Spildooren J, et al. Cognitive aspects of freezing of gait in Parkinson’s disease: a challenge for rehabilitation. J Neural Transm. 2013;120(4):543–57. This paper reviews the evidence on cognitive disturbance related to FOG.
64.
go back to reference Naismith SL, Shine JM, Lewis SJ. The specific contributions of set-shifting to freezing of gait in Parkinson’s disease. Mov Disord. 2010;25:1000–4.PubMedCrossRef Naismith SL, Shine JM, Lewis SJ. The specific contributions of set-shifting to freezing of gait in Parkinson’s disease. Mov Disord. 2010;25:1000–4.PubMedCrossRef
65.
go back to reference Vandenbossche J, Deroost N, Soetens E, et al. Freezing of gait in Parkinson disease is associated with impaired conflict resolution. Neurorehabil Neural Repair. 2011;25:765–73.PubMedCrossRef Vandenbossche J, Deroost N, Soetens E, et al. Freezing of gait in Parkinson disease is associated with impaired conflict resolution. Neurorehabil Neural Repair. 2011;25:765–73.PubMedCrossRef
66.
go back to reference Vandenbossche J, Deroost N, Soetens E, et al. Conflict and freezing of gait in Parkinson’s disease: support for a response control deficit. Neuroscience. 2012;206:144–54.PubMedCrossRef Vandenbossche J, Deroost N, Soetens E, et al. Conflict and freezing of gait in Parkinson’s disease: support for a response control deficit. Neuroscience. 2012;206:144–54.PubMedCrossRef
67.
go back to reference Bartels AL, Leenders KL. Brain imaging in patients with freezing of gait. Mov Disord. 2008;23 Suppl 2:S461–7.PubMedCrossRef Bartels AL, Leenders KL. Brain imaging in patients with freezing of gait. Mov Disord. 2008;23 Suppl 2:S461–7.PubMedCrossRef
68.
go back to reference Kostic VS, Agosta F, Pievani M, et al. Pattern of brain tissue loss associated with freezing of gait in Parkinson disease. Neurology. 2012;78:409–16.PubMedCrossRef Kostic VS, Agosta F, Pievani M, et al. Pattern of brain tissue loss associated with freezing of gait in Parkinson disease. Neurology. 2012;78:409–16.PubMedCrossRef
69.
go back to reference Sohn MH, Ursu S, Anderson JR, et al. The role of prefrontal cortex and posterior parietal cortex in task switching. Proc Natl Acad Sci USA. 2000;97:13448–53.PubMedCrossRef Sohn MH, Ursu S, Anderson JR, et al. The role of prefrontal cortex and posterior parietal cortex in task switching. Proc Natl Acad Sci USA. 2000;97:13448–53.PubMedCrossRef
70.
go back to reference Tessitore A, Amboni M, Cirillo G, et al. Regional gray matter atrophy in patients with Parkinson disease and freezing of gait. Am J Neuroradiol. 2012;33:1804–9.PubMedCrossRef Tessitore A, Amboni M, Cirillo G, et al. Regional gray matter atrophy in patients with Parkinson disease and freezing of gait. Am J Neuroradiol. 2012;33:1804–9.PubMedCrossRef
71.
go back to reference Ferreira LK, Busatto GF. Resting-state functional connectivity in normal brain aging. Neurosci Biobehav Rev. 2013;37(3):384–400. Ferreira LK, Busatto GF. Resting-state functional connectivity in normal brain aging. Neurosci Biobehav Rev. 2013;37(3):384–400.
72.
go back to reference Tessitore A, Amboni M, Esposito F, et al. Resting-state brain connectivity in patients with Parkinson's disease and freezing of gait. Parkinsonism Relat Disord. 2012;18:781–7.PubMedCrossRef Tessitore A, Amboni M, Esposito F, et al. Resting-state brain connectivity in patients with Parkinson's disease and freezing of gait. Parkinsonism Relat Disord. 2012;18:781–7.PubMedCrossRef
73.
go back to reference Imamura K, Okayasu N, Nagatsu T. Cerebral blood flow and freezing of gait in Parkinson’s disease. Acta Neurol Scand. 2012;126:210–8.PubMedCrossRef Imamura K, Okayasu N, Nagatsu T. Cerebral blood flow and freezing of gait in Parkinson’s disease. Acta Neurol Scand. 2012;126:210–8.PubMedCrossRef
74.
go back to reference Smith Y, Wichmann T, Factor SA, et al. Parkinson's disease therapeutics: new developments and challenges since the introduction of levodopa. Neuropsychopharmacology. 2012;37:213–46.PubMedCrossRef Smith Y, Wichmann T, Factor SA, et al. Parkinson's disease therapeutics: new developments and challenges since the introduction of levodopa. Neuropsychopharmacology. 2012;37:213–46.PubMedCrossRef
75.
go back to reference Hausdorff JM, Gruendlinger L, Scollins L, et al. Deep brain stimulation effects on gait variability in Parkinson's disease. Mov Disord. 2009;24:1688–92.PubMedCrossRef Hausdorff JM, Gruendlinger L, Scollins L, et al. Deep brain stimulation effects on gait variability in Parkinson's disease. Mov Disord. 2009;24:1688–92.PubMedCrossRef
76.
go back to reference Lohnes CA, Earhart GM. Effect of subthalamic deep brain stimulation on turning kinematics and related saccadic eye movements in Parkinson disease. Exp Neurol. 2012;236:389–94.PubMedCrossRef Lohnes CA, Earhart GM. Effect of subthalamic deep brain stimulation on turning kinematics and related saccadic eye movements in Parkinson disease. Exp Neurol. 2012;236:389–94.PubMedCrossRef
77.
go back to reference McNeely ME, Earhart GM. Medication and subthalamic nucleus deep brain stimulation similarly improve balance and complex gait in Parkinson disease. Parkinsonism Relat Disord. 2013;19:86–91.PubMedCrossRef McNeely ME, Earhart GM. Medication and subthalamic nucleus deep brain stimulation similarly improve balance and complex gait in Parkinson disease. Parkinsonism Relat Disord. 2013;19:86–91.PubMedCrossRef
78.
go back to reference Fasano A, Herzog J, Seifert E, et al. Modulation of gait coordination by subthalamic stimulation improves freezing of gait. Mov Disord. 2011;26:844–51.PubMedCrossRef Fasano A, Herzog J, Seifert E, et al. Modulation of gait coordination by subthalamic stimulation improves freezing of gait. Mov Disord. 2011;26:844–51.PubMedCrossRef
79.
go back to reference • Espay AJ, Fasano A, van Nuenen BFL, et al. “On” state freezing of gait in Parkinson disease: a paradoxical levodopa-induced complication. Neurology. 2012;78:454–7. This paper proposes 3 subtypes of freezing of gait based on their responsiveness to levodopa.PubMedCrossRef • Espay AJ, Fasano A, van Nuenen BFL, et al. “On” state freezing of gait in Parkinson disease: a paradoxical levodopa-induced complication. Neurology. 2012;78:454–7. This paper proposes 3 subtypes of freezing of gait based on their responsiveness to levodopa.PubMedCrossRef
80.
go back to reference Malkani R, Zadikoff C, Melen O, et al. Amantadine for freezing of gait in patients with Parkinson disease. Clin Neuropharmacol. 2012;35:266–8.PubMedCrossRef Malkani R, Zadikoff C, Melen O, et al. Amantadine for freezing of gait in patients with Parkinson disease. Clin Neuropharmacol. 2012;35:266–8.PubMedCrossRef
81.
go back to reference Kim YE, Yun JY, Yang HJ, et al. Intravenous amantadine for freezing of gait resistant to dopaminergic therapy: a randomized, double-blind, placebo-controlled, cross-over clinical trial. PLoS One. 2012;7:e48890.PubMedCrossRef Kim YE, Yun JY, Yang HJ, et al. Intravenous amantadine for freezing of gait resistant to dopaminergic therapy: a randomized, double-blind, placebo-controlled, cross-over clinical trial. PLoS One. 2012;7:e48890.PubMedCrossRef
82.
go back to reference Moreau C, Defebvre L, Devos D, et al. STN vs PPN-DBS for alleviating freezing of gait: toward a frequency modulation approach? Mov Disord. 2009;24:2164–6.PubMedCrossRef Moreau C, Defebvre L, Devos D, et al. STN vs PPN-DBS for alleviating freezing of gait: toward a frequency modulation approach? Mov Disord. 2009;24:2164–6.PubMedCrossRef
83.
go back to reference Xie T, Kang UJ, Warnke P. Effect of stimulation frequency on immediate freezing of gait in newly activated STN DBS in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2012;83:015–7.CrossRef Xie T, Kang UJ, Warnke P. Effect of stimulation frequency on immediate freezing of gait in newly activated STN DBS in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2012;83:015–7.CrossRef
84.
go back to reference Brozova H, Barnaure I, Alterman RL, et al. STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology. 2009;72:770–1.PubMedCrossRef Brozova H, Barnaure I, Alterman RL, et al. STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology. 2009;72:770–1.PubMedCrossRef
85.
86.
go back to reference Niu L, Ji LY, Li JM, et al. Effect of bilateral deep brain stimulation of the subthalamic nucleus on freezing of gait in Parkinson's disease. J Int Med Res. 2012;40:1108–13.PubMedCrossRef Niu L, Ji LY, Li JM, et al. Effect of bilateral deep brain stimulation of the subthalamic nucleus on freezing of gait in Parkinson's disease. J Int Med Res. 2012;40:1108–13.PubMedCrossRef
87.
go back to reference Moreau C, Delval A, Defebvre L, et al. Methylphenidate for gait hypokinesia and freezing in patients with Parkinson’s disease undergoing subthalamic stimulation: a multicenter, parallel, randomized, placebo-controlled trial. Lancet Neurol. 2012;11:589–96.PubMedCrossRef Moreau C, Delval A, Defebvre L, et al. Methylphenidate for gait hypokinesia and freezing in patients with Parkinson’s disease undergoing subthalamic stimulation: a multicenter, parallel, randomized, placebo-controlled trial. Lancet Neurol. 2012;11:589–96.PubMedCrossRef
88.
go back to reference Espay AJ, Dwivedi AK, Payne M, et al. Methylphenidate for gait impairment in Parkinson disease: a randomized clinical trial. Neurology. 2011;76:1256–62.PubMedCrossRef Espay AJ, Dwivedi AK, Payne M, et al. Methylphenidate for gait impairment in Parkinson disease: a randomized clinical trial. Neurology. 2011;76:1256–62.PubMedCrossRef
89.
go back to reference Braak H, Bohl JR, Müller CM, et al. Stanley Fahn Lecture, 2005: the staging procedure for the inclusion body pathology associated with sporadic Parkinson's disease reconsidered. Mov Disord. 2006;21:2042–51.PubMedCrossRef Braak H, Bohl JR, Müller CM, et al. Stanley Fahn Lecture, 2005: the staging procedure for the inclusion body pathology associated with sporadic Parkinson's disease reconsidered. Mov Disord. 2006;21:2042–51.PubMedCrossRef
90.
go back to reference Grimbergen YAM, Langston JW, Roos RAC, et al. Postural instability in Parkinson’s disease: the adrenergic hypothesis and the locus coeruleus. Exp Rev Neurother. 2007;9:279–90.CrossRef Grimbergen YAM, Langston JW, Roos RAC, et al. Postural instability in Parkinson’s disease: the adrenergic hypothesis and the locus coeruleus. Exp Rev Neurother. 2007;9:279–90.CrossRef
91.
go back to reference Devos D, Defebvre L, Bordet R. Dopaminergic and nondopaminergic pharmacological hypotheses for gait disorders in Parkinson's disease. Fundam Clin Pharmacol. 2010;24:407–21.PubMedCrossRef Devos D, Defebvre L, Bordet R. Dopaminergic and nondopaminergic pharmacological hypotheses for gait disorders in Parkinson's disease. Fundam Clin Pharmacol. 2010;24:407–21.PubMedCrossRef
92.
go back to reference Narabayashi H, Kondo T, Yokochi F, et al. Clinical effects of L-threo-3,4-dihydroxyphenylserine in cases of parkinsonism and pure akinesia. Adv Neurol. 1987;45:593–602.PubMed Narabayashi H, Kondo T, Yokochi F, et al. Clinical effects of L-threo-3,4-dihydroxyphenylserine in cases of parkinsonism and pure akinesia. Adv Neurol. 1987;45:593–602.PubMed
93.
go back to reference Martinez-Gonzalez C, Bolam JP, Mena-Segovia J. Topographical organization of the pedunculopontine nucleus. Front Neuroanat. 2011;5:22.PubMedCrossRef Martinez-Gonzalez C, Bolam JP, Mena-Segovia J. Topographical organization of the pedunculopontine nucleus. Front Neuroanat. 2011;5:22.PubMedCrossRef
94.
go back to reference Aravamuthan BR, Muthusamy KA, Stein JF, et al. Topography of cortical and subcortical connections of the human pedunculopontine and subthalamic nuclei. Neuroimage. 2007;37:694–705.PubMedCrossRef Aravamuthan BR, Muthusamy KA, Stein JF, et al. Topography of cortical and subcortical connections of the human pedunculopontine and subthalamic nuclei. Neuroimage. 2007;37:694–705.PubMedCrossRef
95.
go back to reference Ballanger B, Lozano AM, Moro E, et al. Cerebral blood flow changes induced by pedunculopontine nucleus stimulation in patients with advanced Parkinson's disease: a [(15)O] H2O PET study. Hum Brain Mapp. 2009;30:3901–9.PubMedCrossRef Ballanger B, Lozano AM, Moro E, et al. Cerebral blood flow changes induced by pedunculopontine nucleus stimulation in patients with advanced Parkinson's disease: a [(15)O] H2O PET study. Hum Brain Mapp. 2009;30:3901–9.PubMedCrossRef
96.
go back to reference Tsang EW, Hamani C, Moro E, et al. Involvement of the human pedunculopontine nucleus region in voluntary movements. Neurology. 2010;75:950–9.PubMedCrossRef Tsang EW, Hamani C, Moro E, et al. Involvement of the human pedunculopontine nucleus region in voluntary movements. Neurology. 2010;75:950–9.PubMedCrossRef
97.
go back to reference Jahn K, Deutschländer A, Stephan T, et al. Imaging human supraspinal locomotor centers in brainstem and cerebellum. Neuroimage. 2008;39:786–92.PubMedCrossRef Jahn K, Deutschländer A, Stephan T, et al. Imaging human supraspinal locomotor centers in brainstem and cerebellum. Neuroimage. 2008;39:786–92.PubMedCrossRef
98.
go back to reference Tykocki T, Mandat T, Nauman P. Pedunculopontine nucleus deep brain stimulation in Parkinson’s disease. Arch Med Sci. 2011;4:555–64.CrossRef Tykocki T, Mandat T, Nauman P. Pedunculopontine nucleus deep brain stimulation in Parkinson’s disease. Arch Med Sci. 2011;4:555–64.CrossRef
99.
go back to reference Ferraye MU, Debû B, Fraix V, et al. Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson's disease. Brain. 2010;133:205–14.PubMedCrossRef Ferraye MU, Debû B, Fraix V, et al. Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson's disease. Brain. 2010;133:205–14.PubMedCrossRef
100.
go back to reference Yarnall A, Rochester L, Burn DJ. The interplay of cholinergic function, attention, and falls in Parkinson's disease. Mov Disord. 2011;26:2496–503.PubMedCrossRef Yarnall A, Rochester L, Burn DJ. The interplay of cholinergic function, attention, and falls in Parkinson's disease. Mov Disord. 2011;26:2496–503.PubMedCrossRef
Metadata
Title
Freezing of Gait in Parkinson’s Disease: Where Are We Now?
Authors
Elke Heremans
Alice Nieuwboer
Sarah Vercruysse
Publication date
01-06-2013
Publisher
Current Science Inc.
Published in
Current Neurology and Neuroscience Reports / Issue 6/2013
Print ISSN: 1528-4042
Electronic ISSN: 1534-6293
DOI
https://doi.org/10.1007/s11910-013-0350-7

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