Skip to main content
Erschienen in: Journal of Neurology 5/2014

01.05.2014 | Original Communication

Reduced StartReact effect and freezing of gait in Parkinson’s disease: two of a kind?

verfasst von: Jorik Nonnekes, Alexander C. H. Geurts, Lars B. Oude Nijhuis, Karin van Geel, Anke H. Snijders, Bastiaan R. Bloem, Vivian Weerdesteyn

Erschienen in: Journal of Neurology | Ausgabe 5/2014

Einloggen, um Zugang zu erhalten

Abstract

Freezing of gait (FOG) is a disabling feature of Parkinson’s disease. Emerging evidence suggests that dysfunction of the pedunculopontine nucleus (PPN) and pontomedullary reticular formation (pmRF) plays a role in the causation of FOG. These brainstem structures can be examined by the StartReact paradigm, which utilizes a startling stimulus to accelerate reaction times (StartReact). Here, we examined gait initiation in PD patients with and without FOG using this paradigm. Twenty-six patients with Parkinson’s disease (12 freezers and 14 non-freezers) and 15 controls performed two tasks: rapid gait initiation in response to an imperative ‘go’ signal; and a control condition, involving a simple reaction-time task involving ankle dorsiflexion. During both tasks, a startling acoustic stimulus was combined with the imperative signal in 25 % of trials. In controls, the startle accelerated gait initiation and shortened the onset latency of tibialis anterior responses during ankle dorsiflexion. This acceleration was intact in non-freezers, but was significantly attenuated in the freezers. Independent of the occurrence of a startle, freezers showed a reduced length of the first step compared to non-freezers and controls. The diminished StartReact effect in freezers probably reflects deficient representation or release of motor programs at the brainstem reticular level due to dysfunction of the PPN, the pmRF, or both. These brainstem structures are presumably involved in integrating anticipatory postural adjustments with subsequent stepping movements. We suggest that with time-varying demands, these structures may no longer be able to coordinate the integration of anticipatory postural adjustments with steps, leading to FOG episodes.
Literatur
1.
Zurück zum Zitat 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 19:871–884CrossRefPubMed 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 19:871–884CrossRefPubMed
2.
Zurück zum Zitat Burleigh-Jacobs A, Horak FB, Nutt JG, Obeso JA (1997) Step initiation in Parkinson’s disease: influence of levodopa and external sensory triggers. Mov Disord 12:206–215CrossRefPubMed Burleigh-Jacobs A, Horak FB, Nutt JG, Obeso JA (1997) Step initiation in Parkinson’s disease: influence of levodopa and external sensory triggers. Mov Disord 12:206–215CrossRefPubMed
3.
Zurück zum Zitat Carlsen AN, Almeida QJ, Franks IM (2013) Using a startling acoustic stimulus to investigate underlying mechanisms of bradykinesia in Parkinson’s disease. Neuropsychologia 51:392–399CrossRefPubMed Carlsen AN, Almeida QJ, Franks IM (2013) Using a startling acoustic stimulus to investigate underlying mechanisms of bradykinesia in Parkinson’s disease. Neuropsychologia 51:392–399CrossRefPubMed
4.
Zurück zum Zitat Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004) Prepared movements are elicited early by startle. J Mot Behav 36:253–264CrossRefPubMed Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004) Prepared movements are elicited early by startle. J Mot Behav 36:253–264CrossRefPubMed
5.
Zurück zum Zitat Carpenter MG, Allum JH, Honegger F, Adkin AL, Bloem BR (2004) Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiatry 75:1245–1254PubMedCentralCrossRefPubMed Carpenter MG, Allum JH, Honegger F, Adkin AL, Bloem BR (2004) Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiatry 75:1245–1254PubMedCentralCrossRefPubMed
6.
Zurück zum Zitat Chee R, Murphy A, Danoudis M, Georgiou-Karistianis N, Iansek R (2009) Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain 132:2151–2160CrossRefPubMed Chee R, Murphy A, Danoudis M, Georgiou-Karistianis N, Iansek R (2009) Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain 132:2151–2160CrossRefPubMed
8.
Zurück zum Zitat Davis RB, Ounpuu S, Tyburski D, Gage JR (1991) A gait analysis data-collection and reduction technique. Hum Mov Sci 10:575–587CrossRef Davis RB, Ounpuu S, Tyburski D, Gage JR (1991) A gait analysis data-collection and reduction technique. Hum Mov Sci 10:575–587CrossRef
9.
Zurück zum Zitat Fernandez-Del-Olmo M, Bello O, Lopez-Alonso V, Andres Sanchez J, Santos-Garcia D, Valls-Sole J (2012) The effects of auditory startle and nonstartle stimuli on step initiation in Parkinson’s disease. Mov Disord 27:1570–1573CrossRefPubMed Fernandez-Del-Olmo M, Bello O, Lopez-Alonso V, Andres Sanchez J, Santos-Garcia D, Valls-Sole J (2012) The effects of auditory startle and nonstartle stimuli on step initiation in Parkinson’s disease. Mov Disord 27:1570–1573CrossRefPubMed
10.
Zurück zum Zitat Gantchev N, Viallet F, Aurenty R, Massion J (1996) Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr Clin Neurophysiol 101:110–120CrossRefPubMed Gantchev N, Viallet F, Aurenty R, Massion J (1996) Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping movements in parkinsonian patients. Electroencephalogr Clin Neurophysiol 101:110–120CrossRefPubMed
11.
Zurück zum Zitat Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N, Movement Disorder Society URTF (2008) Movement disorder society-sponsored revision of the unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRefPubMed Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N, Movement Disorder Society URTF (2008) Movement disorder society-sponsored revision of the unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRefPubMed
12.
Zurück zum Zitat Hanakawa T, Katsumi Y, Fukuyama H, Honda M, Hayashi T, Kimura J, Shibasaki H (1999) Mechanisms underlying gait disturbance in Parkinson’s disease: a single photon emission computed tomography study. Brain 122(Pt 7):1271–1282CrossRefPubMed Hanakawa T, Katsumi Y, Fukuyama H, Honda M, Hayashi T, Kimura J, Shibasaki H (1999) Mechanisms underlying gait disturbance in Parkinson’s disease: a single photon emission computed tomography study. Brain 122(Pt 7):1271–1282CrossRefPubMed
13.
Zurück zum Zitat Hausdorff JM, Schaafsma JD, Balash Y, Bartels AL, Gurevich T, Giladi N (2003) Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res 149:187–194PubMed Hausdorff JM, Schaafsma JD, Balash Y, Bartels AL, Gurevich T, Giladi N (2003) Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res 149:187–194PubMed
14.
Zurück zum Zitat Inglis WL, Winn P (1995) The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog Neurobiol 47:1–29CrossRefPubMed Inglis WL, Winn P (1995) The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog Neurobiol 47:1–29CrossRefPubMed
15.
Zurück zum Zitat Koch M, Kungel M, Herbert H (1993) Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat. Exp Brain Res 97:71–82CrossRefPubMed Koch M, Kungel M, Herbert H (1993) Cholinergic neurons in the pedunculopontine tegmental nucleus are involved in the mediation of prepulse inhibition of the acoustic startle response in the rat. Exp Brain Res 97:71–82CrossRefPubMed
16.
Zurück zum Zitat la Fougere C, Zwergal A, Rominger A, Forster S, Fesl G, Dieterich M, Brandt T, Strupp M, Bartenstein P, Jahn K (2010) Real versus imagined locomotion: a [18F]-FDG PET-fMRI comparison. Neuroimage 50:1589–1598CrossRefPubMed la Fougere C, Zwergal A, Rominger A, Forster S, Fesl G, Dieterich M, Brandt T, Strupp M, Bartenstein P, Jahn K (2010) Real versus imagined locomotion: a [18F]-FDG PET-fMRI comparison. Neuroimage 50:1589–1598CrossRefPubMed
17.
Zurück zum Zitat Mille ML, Johnson Hilliard M, Martinez KM, Simuni T, Rogers MW (2007) Acute effects of a lateral postural assist on voluntary step initiation in patients with Parkinson’s disease. Mov Disord 22:20–27CrossRefPubMed Mille ML, Johnson Hilliard M, Martinez KM, Simuni T, Rogers MW (2007) Acute effects of a lateral postural assist on voluntary step initiation in patients with Parkinson’s disease. Mov Disord 22:20–27CrossRefPubMed
18.
19.
Zurück zum Zitat Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Fieuws S, Broens-Kaucsik E (2001) Abnormalities of the spatiotemporal characteristics of gait at the onset of freezing in Parkinson’s disease. Mov Disord 16:1066–1075CrossRefPubMed Nieuwboer A, Dom R, De Weerdt W, Desloovere K, Fieuws S, Broens-Kaucsik E (2001) Abnormalities of the spatiotemporal characteristics of gait at the onset of freezing in Parkinson’s disease. Mov Disord 16:1066–1075CrossRefPubMed
20.
Zurück zum Zitat Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, Giladi N (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their careers. Gait Posture 30:459–463CrossRefPubMed Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, Giladi N (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their careers. Gait Posture 30:459–463CrossRefPubMed
21.
Zurück zum Zitat Nonnekes J, Oude Nijhuis LB, de Niet M, de Bot ST, Pasman JW, van de Warrenburg BP, Bloem BR, Weerdesteyn V, Geurts AC (2014) StartReact restores reaction time in HSP: evidence for subcortical release of a motor program. J Neurosci 34:275–281CrossRefPubMed Nonnekes J, Oude Nijhuis LB, de Niet M, de Bot ST, Pasman JW, van de Warrenburg BP, Bloem BR, Weerdesteyn V, Geurts AC (2014) StartReact restores reaction time in HSP: evidence for subcortical release of a motor program. J Neurosci 34:275–281CrossRefPubMed
22.
Zurück zum Zitat Nonnekes J, Scotti A, Oude Nijhuis LB, Smulders K, Queralt A, Geurts AC et al (2013) Are postural responses to backward and forward perturbations processed by different neural circuits? Neuroscience 245:109–120 Nonnekes J, Scotti A, Oude Nijhuis LB, Smulders K, Queralt A, Geurts AC et al (2013) Are postural responses to backward and forward perturbations processed by different neural circuits? Neuroscience 245:109–120
23.
Zurück zum Zitat 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 10:734–744CrossRefPubMed 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 10:734–744CrossRefPubMed
24.
Zurück zum Zitat Queralt A, Weerdesteyn V, van Duijnhoven HJ, Castellote JM, Valls-Sole J, Duysens J (2008) The effects of an auditory startle on obstacle avoidance during walking. J Physiol 586:4453–4463PubMedCentralCrossRefPubMed Queralt A, Weerdesteyn V, van Duijnhoven HJ, Castellote JM, Valls-Sole J, Duysens J (2008) The effects of an auditory startle on obstacle avoidance during walking. J Physiol 586:4453–4463PubMedCentralCrossRefPubMed
25.
Zurück zum Zitat Reese NB, Garcia-Rill E, Skinner RD (1995) The pedunculopontine nucleus-auditory input, arousal and pathophysiology. Prog Neurobiol 47:105–133CrossRefPubMed Reese NB, Garcia-Rill E, Skinner RD (1995) The pedunculopontine nucleus-auditory input, arousal and pathophysiology. Prog Neurobiol 47:105–133CrossRefPubMed
26.
Zurück zum Zitat Rogers MW, Kennedy R, Palmer S, Pawar M, Reising M, Martinez KM, Simuni T, Zhang Y, MacKinnon CD (2011) Postural preparation prior to stepping in patients with Parkinson’s disease. J Neurophysiol 106:915–924CrossRefPubMed Rogers MW, Kennedy R, Palmer S, Pawar M, Reising M, Martinez KM, Simuni T, Zhang Y, MacKinnon CD (2011) Postural preparation prior to stepping in patients with Parkinson’s disease. J Neurophysiol 106:915–924CrossRefPubMed
27.
Zurück zum Zitat Schepens B, Stapley P, Drew T (2008) Neurons in the pontomedullary reticular formation signal posture and movement both as an integrated behavior and independently. J Neurophysiol 100:2235–2253CrossRefPubMed Schepens B, Stapley P, Drew T (2008) Neurons in the pontomedullary reticular formation signal posture and movement both as an integrated behavior and independently. J Neurophysiol 100:2235–2253CrossRefPubMed
28.
Zurück zum Zitat Snijders AH (2012) Summary and discussion. In: Tackling freezing of gait in Parkinson’s disease. Ipskamp Drukkers, Enschede, pp 196–197 Snijders AH (2012) Summary and discussion. In: Tackling freezing of gait in Parkinson’s disease. Ipskamp Drukkers, Enschede, pp 196–197
29.
Zurück zum Zitat Snijders AH, Haaxma CA, Hagen YJ, Munneke M, Bloem BR (2012) Freezer or non-freezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord 18:149–154CrossRefPubMed Snijders AH, Haaxma CA, Hagen YJ, Munneke M, Bloem BR (2012) Freezer or non-freezer: clinical assessment of freezing of gait. Parkinsonism Relat Disord 18:149–154CrossRefPubMed
30.
Zurück zum Zitat 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 134:59–72CrossRefPubMed 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 134:59–72CrossRefPubMed
31.
Zurück zum Zitat Thevathasan W, Cole MH, Graepel CL, Hyam JA, Jenkinson N, Brittain JS, Coyne TJ, Silburn PA, Aziz TZ, Kerr G, Brown P (2012) A spatiotemporal analysis of gait freezing and the impact of pedunculopontine nucleus stimulation. Brain 135:1446–1454PubMedCentralCrossRefPubMed Thevathasan W, Cole MH, Graepel CL, Hyam JA, Jenkinson N, Brittain JS, Coyne TJ, Silburn PA, Aziz TZ, Kerr G, Brown P (2012) A spatiotemporal analysis of gait freezing and the impact of pedunculopontine nucleus stimulation. Brain 135:1446–1454PubMedCentralCrossRefPubMed
32.
Zurück zum Zitat Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Bogdanovic M, Coyne TJ, Silburn PA, Aziz TZ, Brown P (2011) A block to pre-prepared movement in gait freezing, relieved by pedunculopontine nucleus stimulation. Brain 134:2085–2095PubMedCentralCrossRefPubMed Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Bogdanovic M, Coyne TJ, Silburn PA, Aziz TZ, Brown P (2011) A block to pre-prepared movement in gait freezing, relieved by pedunculopontine nucleus stimulation. Brain 134:2085–2095PubMedCentralCrossRefPubMed
33.
Zurück zum Zitat Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Foltynie T, Limousin P, Bogdanovic M, Zrinzo L, Green AL, Aziz TZ, Brown P (2012) Alpha oscillations in the pedunculopontine nucleus correlate with gait performance in parkinsonism. Brain 135:148–160PubMedCentralCrossRefPubMed Thevathasan W, Pogosyan A, Hyam JA, Jenkinson N, Foltynie T, Limousin P, Bogdanovic M, Zrinzo L, Green AL, Aziz TZ, Brown P (2012) Alpha oscillations in the pedunculopontine nucleus correlate with gait performance in parkinsonism. Brain 135:148–160PubMedCentralCrossRefPubMed
34.
Zurück zum Zitat Valls-Sole J, Kumru H, Kofler M (2008) Interaction between startle and voluntary reactions in humans. Exp Brain Res 187:497–507CrossRefPubMed Valls-Sole J, Kumru H, Kofler M (2008) Interaction between startle and voluntary reactions in humans. Exp Brain Res 187:497–507CrossRefPubMed
35.
Zurück zum Zitat Vaugoyeau M, Viallet F, Mesure S, Massion J (2003) Coordination of axial rotation and step execution: deficits in Parkinson’s disease. Gait Posture 18:150–157CrossRefPubMed Vaugoyeau M, Viallet F, Mesure S, Massion J (2003) Coordination of axial rotation and step execution: deficits in Parkinson’s disease. Gait Posture 18:150–157CrossRefPubMed
Metadaten
Titel
Reduced StartReact effect and freezing of gait in Parkinson’s disease: two of a kind?
verfasst von
Jorik Nonnekes
Alexander C. H. Geurts
Lars B. Oude Nijhuis
Karin van Geel
Anke H. Snijders
Bastiaan R. Bloem
Vivian Weerdesteyn
Publikationsdatum
01.05.2014
Verlag
Springer Berlin Heidelberg
Erschienen in
Journal of Neurology / Ausgabe 5/2014
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-014-7304-0

Weitere Artikel der Ausgabe 5/2014

Journal of Neurology 5/2014 Zur Ausgabe

Pioneers in Neurology

Kurt Goldstein (1878–1965)

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.