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Cognitive aspects of freezing of gait in Parkinson’s disease: a challenge for rehabilitation

  • Neurology and Preclinical Neurological Studies - Review Article
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Abstract

Freezing of gait (FOG) is a very disabling symptom affecting up to half of the patients with Parkinson’s disease (PD). Evidence is accumulating that FOG is caused by a complex interplay between motor, cognitive and affective factors, rather than being a pure motor phenomenon. In the current paper, we review the evidence on the specific role of cognitive factors in FOG. Results from behavioral studies show that patients with FOG experience impairments in executive functioning and response selection which predict that motor learning may be compromised. Brain imaging studies strengthen the neural basis of a potential association between FOG and cognitive impairment, but do not clarify whether it is a primary or secondary determinant of FOG. A FOG-related reduction of cognitive resources implies that adaptation of rehabilitation interventions is indicated for patients with FOG to promote the consolidation of learning.

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References

  • Allen NE, Canning CG, Sherrington C, Lord SR, Latt MD, Close JC, O’Rourke SD, Murray SM, Fung VS (2010) The effects of an exercise program on fall risk factors in people with Parkinson’s disease: a randomized controlled trial. Mov Disord 25:1217–1225

    Article  PubMed  Google Scholar 

  • Almeida QJ, Lebold CA (2010) Freezing of gait in Parkinson’s disease: a perceptual cause for a motor impairment? J Neurol Neurosurg Psychiatry 81:513–518

    Article  PubMed  CAS  Google Scholar 

  • Amboni M, Cozzolino A, Longo K, Picillo M, Barone P (2008) Freezing of gait and executive functions in patients with Parkinson’s disease. Mov Disord 23:395–400

    Article  PubMed  Google Scholar 

  • Amboni M, Barone P, Picillo M, Cozzolino A, Longo K, Erro R, Iavarone A (2010) A two-year follow-up of executive dysfunctions in parkinsonian patients with freezing of gait at on-state. Mov Disord 25:800–802

    Article  PubMed  Google Scholar 

  • Arias P, Cudeiro J (2010) Effect of rhythmic auditory stimulation on gait in Parkinsonian patients with and without freezing of gait. PLoS ONE 5:9675

    Article  Google Scholar 

  • Bächlin M, Plotnik M, Roggen D, Giladi N, Hausdorff JM, Tröster G (2010) A wearable system to assist walking of Parkinson s disease patients. Methods Inf Med 49:88–95

    PubMed  Google Scholar 

  • Baddeley AD (2000) The episodic buffer: a new component of working memory? Trends Cogn Sci 4:417–423

    Article  PubMed  Google Scholar 

  • Baddeley AD, Hitch GJ (1974) Working memory. In: Bower GA (ed) The psychology of learning and motivation. Academic Press, New York, pp 47–89

    Google Scholar 

  • Bartels AL, de Jong BM, Giladi N, Schaafsma JD, Maguire RP, Veenma L, Pruim J, Balash Y, Youdim MB, Leenders KL (2006) Striatal dopa and glucose metabolism in PD patients with freezing of gait. Mov Disord 21:1326–1332

    Article  PubMed  Google Scholar 

  • Bloem BR, Hausdorff JM, Visser JE, Giladi N (2004) Falls and freezing of gait in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov Disord 19:871–884

    Article  PubMed  Google Scholar 

  • Brichetto G, Pelosin E, Marchese R, Abbruzzese G (2006) Evaluation of physical therapy in parkinsonian patients with freezing of gait: a pilot study. Clin Rehabil 20:31–35

    Article  PubMed  CAS  Google Scholar 

  • Cohen RG, Chao A, Nutt JG, Horak FB (2011) 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 49:3981–3988

    Article  PubMed  Google Scholar 

  • Cowie D, Limousin P, Peters A, Hariz M, Day BL (2012) Doorway-provoked freezing of gait in Parkinson’s disease. Mov Disord 27:492–499

    Article  PubMed  Google Scholar 

  • Cubo E, Leurgans S, Goetz CG (2004) Short-term and practice effects of metronome pacing in Parkinson’s disease patients with gait freezing while in the ‘on’ state: randomized single blind evaluation. Parkinsonism Relat Disord 10:507–510

    Article  PubMed  Google Scholar 

  • Deroost N, Kerckhofs E, Coene M, Wijnants G, Soetens E (2006) Learning sequence movements in a homogenous sample of patients with Parkinson’s disease. Neuropsychologia 44:1653–1662

    Article  PubMed  Google Scholar 

  • Dietz MA, Goetz CG, Stebbins GT (1990) Evaluation of a modified inverted walking stick as a treatment for parkinsonian freezing episodes. Mov Disord 5:243–247

    Article  PubMed  CAS  Google Scholar 

  • Donovan S, Lim C, Diaz N, Browner N, Rose P, Sudarsky LR, Tarsy D, Fahn S, Simon DK (2011) Laserlight cues for gait freezing in Parkinson’s disease: an open-label study. Parkinsonism Relat Disord 17:240–245

    Article  PubMed  CAS  Google Scholar 

  • Ferraye MU, Debû B, Fraix V, Xie-Brustolin J, Chabardès S, Krack P, Benabid AL, Pollak P (2008) Effects of subthalamic nucleus stimulation and levodopa on freezing of gait in Parkinson disease. Neurology 70:1431–1437

    Article  PubMed  CAS  Google Scholar 

  • Ferraye MU, Debû B, Fraix V, Goetz L, Ardouin C, Yelnik J, Henry-Lagrange C, Seigneuret E, Piallat B, Krack P, Le Bas JF, Benabid AL, Chabardès S, Pollak P (2010) Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson’s disease. Brain 133:205–214

    Article  PubMed  CAS  Google Scholar 

  • Frazzitta G, Maestri R, Uccellini D, Bertotti G, Abelli P (2009) Rehabilitation treatment of gait in patients with Parkinson’s disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord 24:1139–1143

    Article  PubMed  Google Scholar 

  • Giladi N, Hausdorff JM (2006) The role of mental function in the pathogenesis of freezing of gait in Parkinson’s disease. J Neurol Sci 248:173–176

    Article  PubMed  Google Scholar 

  • Giladi N, Nieuwboer A (2008) Understanding and treating freezing of gait in Parkinsonism, proposed working definition and setting the stage. Mov Disord 23:S423–S425

    Article  PubMed  Google Scholar 

  • Griffin HJ, Greenlaw R, Limousin P, Bhatia K, Quinn NP, Jahanshahi M (2011) The effect of real and virtual visual cues on walking in Parkinson’s disease. J Neurol 258:991–1000

    Article  PubMed  CAS  Google Scholar 

  • Hackney ME, Earhart GM (2009) The effects of a secondary task on forward and backward walking in Parkinson’s disease. Neurorehabil Neural Repair [Epub ahead of print]

  • Heremans E, Feys P, Nieuwboer A, Vercruysse S, Vandenberghe W, Sharma N, Helsen WF (2011) Motor imagery ability in patients with early- and mid-stage Parkinson disease. Neurorehabil Neural Repair 25:168–177

    Article  PubMed  Google Scholar 

  • Heremans E, Nieuwboer A, Feys P, Vercruysse S, Vandenberghe W, Sharma N, Helsen WF (2012) External cueing improves motor imagery quality in patients with Parkinson disease. Neurorehabil Neural Repair 26:27–35

    Article  PubMed  Google Scholar 

  • Huang C, Mattis P, Tang C, Perrine K, Carbon M, Eidelberg D (2007) Metabolic brain networks associated with cognitive function in Parkinson’s disease. Neuroimage 34:714–723

    Article  PubMed  Google Scholar 

  • Imamura K, Okayasu N, Nagatsu T (2012) Cerebral blood flow and freezing of gait in Parkinson’s disease. Acta Neurol Scand 126:210–218

    Google Scholar 

  • Kadivar Z, Corcos DM, Foto J, Hondzinski JM (2011) Effect of step training and rhythmic auditory stimulation on functional performance in Parkinson patients. Neurorehabil Neural Repair. 25:626–635

    Article  PubMed  Google Scholar 

  • Kompoliti K, Goetz CG, Leurgans S, Morrissey M, Siegel IM (2000) “On” freezing in Parkinson’s disease: resistance to visual cue walking devices. Mov Disord 15:309–312

    Article  PubMed  CAS  Google Scholar 

  • Kostic VS, Agosta F, Pievani M, Stefanova E, Jecmenica-Lukic M, Scarale A, Spica V, Filippi M (2012) Pattern of brain tissue loss associated with freezing of gait in Parkinson disease. Neurology 78:409–416

    Article  PubMed  CAS  Google Scholar 

  • Kudlicka A, Clare L, Hindle JV (2011) Executive functions in Parkinson’s disease: systematic review and meta-analysis. Mov Disord 26:2305–2315

    Article  PubMed  Google Scholar 

  • Lebold CA, Almeida QJ (2010) Evaluating the contributions of dynamic flow to freezing of gait in Parkinson’s disease. Parkinsons Dis 732508

  • Lee SJ, Yoo JY, Ryu JS, Park HK, Chung SJ (2012) The effects of visual and auditory cues on freezing of gait in patients with Parkinson disease. Am J Phys Med Rehabil 91:2–11

    Article  PubMed  Google Scholar 

  • Lewis SJG, Barker RA (2009) A pathophysiological model of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 15:333–338

    Article  PubMed  Google Scholar 

  • Matsui H, Udaka F, Miyoshi T, Hara N, Tamaura A, Oda M, Kubori T, Nishinaka K, Kameyama M (2005) Three-dimensional stereotactic surface projection study of freezing of gait and brain perfusion image in Parkinson’s disease. Mov Disord 20:1272–1277

    Article  PubMed  Google Scholar 

  • Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD (2000) The unity and diversity of executive functions and their contributions to complex ‘‘Frontal Lobe’’ tasks: a latent variable analysis. Cogn Psychol 41:49–100

    Article  PubMed  CAS  Google Scholar 

  • Moore O, Peretz C, Giladi N (2007) Freezing of gait affects quality of life of peoples with Parkinson’s disease beyond its relationship with mobility and gait. Mov Disord 22:292–295

    Article  Google Scholar 

  • Moreau C, Defebvre L, Bleuse S, Blatt JL, Duhamel A, Bloem BR, Destée A, Krystkowiak P (2008) Externally provoked freezing of gait in open runways in advanced Parkinson’s disease results from motor and mental collapse. J Neural Transm 115:1431–1436

    Article  PubMed  CAS  Google Scholar 

  • Morris ME, Iansek R, Galna B (2008) Gait festination in Parkinson’s disease: pathogenesis and rehabilitation. Mov Disord 23:451–460

    Article  Google Scholar 

  • Morris ME, Iansek R, Kirkwood B (2009) A randomized controlled trial of movement strategies compared with exercise for people with Parkinson’s disease. Mov Disord 24:64–71

    Article  PubMed  Google Scholar 

  • Naismith SL, Shine JM, Lewis SJG (2010) The specific contribution of set-shifting to freezing of gait in Parkinson’s disease. Mov Disord 25:1000–1004

    Article  PubMed  Google Scholar 

  • Nanhoe-Mahabier W, Delval A, Snijders AH, Weerdesteyn V, Overeem S, Bloem BR (2012) The possible price of auditory cueing: influence on obstacle avoidance in Parkinson’s disease. Mov Disord 27:574–578

    Article  PubMed  Google Scholar 

  • Nantel J, McDonald JC, Tan S, Bronte-Stewart H (2012) Deficits in visuospatial processing contribute to quantitative measures of freezing of gait in Parkinson’s disease. Neuroscience 221:151–156

    Article  PubMed  CAS  Google Scholar 

  • Nieuwboer A (2008) Cueing for freezing of gait in patients with Parkinson’s disease: a rehabilitation perspective. Mov Disord 23:S475–S481

    Article  PubMed  Google Scholar 

  • Nieuwboer A, Kwakkel G, Rochester L, Jones D, van Wegen E, Willems AM, Chavret F, Hetherington V, Baker K, Kim I (2007) Cueing training in the home improves gait-related mobility in Parkinson’s disease: the RESCUE trial. J Neurol Neurosurg Psychiatry 78:134–140

    Article  PubMed  CAS  Google Scholar 

  • Nieuwboer A, Baker Willems AM, Jones D, Spildooren J, Lim I, Kwakkel G, Van Wegen E, Rochester L (2009a) The short-term effects of different cueing modalities on turn speed in people with Parkinson’s disease. Neurorehabil Neural Repair 23:831–836

    Article  PubMed  Google Scholar 

  • Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, Giladi N (2009b) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30:459–463

    Article  PubMed  Google Scholar 

  • Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10:734–744

    Article  PubMed  Google Scholar 

  • Pelosin E, Avanzino L, Bove M, Stramesi P, Nieuwboer A, Abbruzzese G (2010) Action observation improves freezing of gait in patients with Parkinson’s disease. Neurorehabil Neural Repair 24:746–752

    Article  PubMed  Google Scholar 

  • Plotnik M, Giladi N, Hausdorff JM (2012) Is freezing of gait in Parkinson’s disease a result of multiple gait impairments? Implications for treatment. Parkinsons Dis (in press)

  • Rahman S, Griffin HJ, Quinn NP, Jahanshahi M (2008) The factors that induce or overcome freezing of gait in Parkinson’s disease. Behav Neurol 19:127–136

    PubMed  CAS  Google Scholar 

  • Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, Bergman H, Agid Y, DeLong MR, Obeso JA (2010) Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease. Nat Rev Neurosci 11:760–772

    Article  PubMed  CAS  Google Scholar 

  • Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM, Giladi N (2003) Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur J Neurol 10:391–398

    Article  PubMed  CAS  Google Scholar 

  • Schweder PM, Hansen PC, Green AL, Quaghebeur G, Stein J, Aziz TZ (2010) Connectivity of the pedunculopontine nucleus in parkinsonian freezing of gait. NeuroReport 21:914–916

    Article  PubMed  Google Scholar 

  • Snijders AH, Nijkrake MJ, Bakker M, Munneke M, Wind C, Bloem BR (2008) Clinimetrics of freezing of gait. Mov Disord 23:S468–S474

    Article  PubMed  Google Scholar 

  • Snijders AH, Leunissen I, Bakker M, Overeem S, Helmich RC, Bloem BR, Toni I (2011) Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain 134:59–72

    Article  PubMed  Google Scholar 

  • Snijders AH, Haaxma CA, Hagen YJ, Munneke M, Bloem BR (2012) Freezer or non-freezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord 18:149–154

    Article  PubMed  Google Scholar 

  • Spildooren J, Vercruysse S, Desloovere K, Vandenberghe W, Kerckhofs E, Nieuwboer A (2010) Freezing of gait in Parkinson’s disease: the impact of dual-tasking and turning. Mov Disord 25:2563–2570

    Article  PubMed  Google Scholar 

  • Spildooren J, Vercruysse S, Meyns P, Vandenbossche J, Heremans E, Desloovere K, Vandenberghe W, Nieuwboer A (2012) Turning and unilateral cueing in Parkinson’s disease patients with and without freezing of gait. Neuroscience 207:298–306

    Article  PubMed  CAS  Google Scholar 

  • Tan DM, McGinley JL, Danoudis ME, Iansek R, Morris ME (2011) Freezing of gait and activity limitations in people with Parkinson’s disease. Arch Phys Med Rehabil 92:1159–1165

    Article  PubMed  Google Scholar 

  • Tessitore A, Amboni M, Esposito F, Russo A, Picillo M, Marcuccio L, Pellecchia MT, Vitale C, Cirillo M, Tedeschi G, Barone P (2012a) Resting-state connectivity in patients with Parkinson’s disease and freezing of gait. Parkinsonism Relat Disord 18:781–787

  • 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 (2012b) Regional gray matter atrophy in patients with Parkinson’s disease and freezing of gait. Am J Neurolradiol 33:1804–1809

  • Thevathasan W, Coyne TJ, Hyam JA, Kerr G, Jenkinson N, Aziz TZ, Silburn PA (2011) Pedunculopontine nucleus stimulation improves gait freezing in Parkinson disease. Neurosurgery 69:1248–1253

    Article  PubMed  Google Scholar 

  • Vandenbossche J, Deroost N, Soetens E, Kerckhofs E (2009) Does implicit learning in non-demented Parkinson’s disease depend on the level of cognitive functioning? Brain Cogn 69:194–199

    Article  PubMed  Google Scholar 

  • Vandenbossche J, Deroost N, Soetens E, Spildooren J, Vercruysse S, Nieuwboer A, Kerckhofs E (2011) Freezing of gait in Parkinson disease is associated with impaired conflict resolution. Neurorehabil Neural Repair 25:765–773

    Article  PubMed  Google Scholar 

  • Vandenbossche J, Deroost N, Soetens E, Coomans D, Spildooren J, Vercruysse S, Nieuwboer A, Kerckhofs E (2012a) Impaired implicit sequence learning in Parkinson’s disease patients with freezing of gait (in press)

  • Vandenbossche J, Deroost N, Soetens E, Zeischka P, Spildooren J, Vercruysse S, Nieuwboer A, Kerckhofs E (2012b) Conflict and freezing of gait in Parkinson’s disease: support for a response control deficit. Neuroscience 206:144–154

    Article  PubMed  CAS  Google Scholar 

  • Vercruysse S, Spildooren J, Heremans E, Vandenbossche J, Levin O, Wenderoth N, Swinnen SP, Janssens L, Vandenberghe W, Nieuwboer A (2012a) Freezing in Parkinson’s disease: a spatiotemporal motor disorder beyond gait. Mov Disord 27:254–263

    Article  PubMed  Google Scholar 

  • Vercruysse S, Devos H, Munks L, Spildooren J, Vandenbossche J, Vandenberghe W, Nieuwboer A, Heremans E (2012b). Explaining freezing of gait in Parkinson’s disease: motor and cognitive determinants. Mov Disord 27:1644–1651

  • Vercruysse S, Spildooren J, Heremans E, Vandenbossche J, Wenderoth N, Swinnen SP, Vandenberghe W, Nieuwboer A (2012c) Abnormalities and cue dependency of rhythmical upper-limb movements in Parkinson patients with freezing of gait. Neurorehabil Neural Repair 26:636–645

    Article  PubMed  Google Scholar 

  • Willems AM, Nieuwboer A, Chavret F, Desloovere K, Dom R, Rochester L, Jones D, Kwakkel G, Van Wegen E (2006) The use of rhythmic auditory cues to influence gait in patients with Parkinson’s disease, the differential effect for freezers and non-freezers, an explorative study. Disabil Rehabil 28:721–728

    Article  PubMed  CAS  Google Scholar 

  • Yarnall A, Rochester L, Burn DJ (2011) The interplay of holinergic function, attention, and falls in Parkinson’s disease. Mov Disord 26:2496–2503

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Rehabilitation Sciences, Katholieke Universiteit Leuven, Tervuursevest 101, 3001, Heverlee, Belgium

    Elke Heremans, A. Nieuwboer, J. Spildooren & S. Vercruysse

  2. Cognitive Psychology, Vrije Universiteit Brussel, Brussels, Belgium

    J. Vandenbossche, N. Deroost, E. Soetens & E. Kerckhofs

Authors
  1. Elke Heremans
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  2. A. Nieuwboer
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  3. J. Spildooren
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  4. J. Vandenbossche
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  5. N. Deroost
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  6. E. Soetens
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  7. E. Kerckhofs
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  8. S. Vercruysse
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Correspondence to Elke Heremans.

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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 120, 543–557 (2013). https://doi.org/10.1007/s00702-012-0964-y

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  • DOI: https://doi.org/10.1007/s00702-012-0964-y

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