Gait and Postural Disorders in REM Sleep Behavior Disorder

  • Colum D. MacKinnonEmail author
  • Laila Alibiglou
  • Aleksandar Videnovic


REM sleep behavior disorder (RBD) is a parasomnia characterized by alterations in the regulation of muscle tone during REM sleep, often in conjunction with dream enactment. RBD is of importance from both a clinical and basic science perspective since individuals diagnosed with RBD have an almost 80% risk of developing Parkinson’s disease (PD) or other α-synuclein-related disorders within one decade. For this reason, studying RBD provides an opportunity to improve our understanding of premotor stages of PD and related synucleinopathies. Moreover, the progression of RBD to RBD with PD is associated with the development of an akinetic-rigid subtype of PD that is often associated with a high risk of falls, gait disturbances, and the development of freezing of gait (FOG). This chapter summarizes the literature showing that the expression of RBD alone is associated with subtle changes in movement control, particularly in the domain of postural stability and gait. Some of the motor features of RBD are akin to distinct abnormalities in posture-locomotion coupling and muscle activation seen in PD with FOG. The possible neural substrates of these impairments are also discussed.


Gait Postural stability Freezing of gait Parkinson’s disease REM sleep behavior disorder 


  1. 1.
    Schenck CH, Bundlie SR, Ettinger MG, Mahowald MW. Chronic behavioral disorders of human REM sleep: a new category of parasomnia. Sleep. 1986;9(2):293–308.CrossRefGoogle Scholar
  2. 2.
    Boeve BF, Silber MH, Saper CB, Ferman TJ, Dickson DW, Parisi JE, et al. Pathophysiology of REM sleep behaviour disorder and relevance to neurodegenerative disease. Brain. 2007;130(Pt 11):2770–88.CrossRefGoogle Scholar
  3. 3.
    Schenck CH, Boeve BF, Mahowald MW. Delayed emergence of a parkinsonian disorder or dementia in 81% of older men initially diagnosed with idiopathic rapid eye movement sleep behavior disorder: a 16-year update on a previously reported series. Sleep Med. 2013;14(8):744–8.CrossRefGoogle Scholar
  4. 4.
    Garcia-Rill E, Houser CR, Skinner RD, Smith W, Woodward DJ. Locomotion-inducing sites in the vicinity of the pedunculopontine nucleus. Brain Res Bull. 1987;18(6):731–8.CrossRefGoogle Scholar
  5. 5.
    Takakusaki K, Saitoh K, Harada H, Okumura T, Sakamoto T. Evidence for a role of basal ganglia in the regulation of rapid eye movement sleep by electrical and chemical stimulation for the pedunculopontine tegmental nucleus and the substantia nigra pars reticulata in decerebrate cats. Neuroscience. 2004;124(1):207–20.CrossRefGoogle Scholar
  6. 6.
    Takakusaki K, Tomita N, Yano M. Substrates for normal gait and pathophysiology of gait disturbances with respect to the basal ganglia dysfunction. J Neurol. 2008;255(Suppl 4):19–29.CrossRefGoogle Scholar
  7. 7.
    Le Ray D, Juvin L, Ryczko D, Dubuc R. Chapter 4–supraspinal control of locomotion: the mesencephalic locomotor region. Prog Brain Res. 2011;188:51–70.CrossRefGoogle Scholar
  8. 8.
    Takakusaki K. Functional neuroanatomy for posture and gait control. J Mov Disord. 2017;10(1):1–17.CrossRefGoogle Scholar
  9. 9.
    Jordan LM, Liu J, Hedlund PB, Akay T, Pearson KG. Descending command systems for the initiation of locomotion in mammals. Brain Res Rev. 2008;57(1):183–91.CrossRefGoogle Scholar
  10. 10.
    Steriade M, Datta S, Pare D, Oakson G, Curro Dossi RC. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci. 1990;10(8):2541–59.CrossRefGoogle Scholar
  11. 11.
    Hirata A, Aguilar J, Castro-Alamancos MA. Noradrenergic activation amplifies bottom-up and top-down signal-to-noise ratios in sensory thalamus. J Neurosci. 2006;26(16):4426–36.CrossRefGoogle Scholar
  12. 12.
    Hirata A, Castro-Alamancos MA. Neocortex network activation and deactivation states controlled by the thalamus. J Neurophysiol. 2010;103(3):1147–57.CrossRefGoogle Scholar
  13. 13.
    Garcia-Rill E, Homma Y, Skinner RD. Arousal mechanisms related to posture and locomotion: 1. Descending modulation. Prog Brain Res. 2004;143:283–90.PubMedGoogle Scholar
  14. 14.
    Takakusaki K, Obara K, Nozu T, Okumura T. Modulatory effects of the GABAergic basal ganglia neurons on the PPN and the muscle tone inhibitory system in cats. Arch Ital Biol. 2011;149(4):385–405.PubMedGoogle Scholar
  15. 15.
    Weng FJ, Williams RH, Hawryluk JM, Lu J, Scammell TE, Saper CB, et al. Carbachol excites sublaterodorsal nucleus neurons projecting to the spinal cord. J Physiol. 2014;592(Pt 7):1601–17.CrossRefGoogle Scholar
  16. 16.
    Semba K. Aminergic and cholinergic afferents to REM sleep induction regions of the pontine reticular formation in the rat. J Comp Neurol. 1993;330(4):543–56.CrossRefGoogle Scholar
  17. 17.
    Goetz L, Piallat B, Bhattacharjee M, Mathieu H, David O, Chabardes S. The primate pedunculopontine nucleus region: towards a dual role in locomotion and waking state. J Neural Transm (Vienna). 2016;123(7):667–78.CrossRefGoogle Scholar
  18. 18.
    Hirsch EC, Graybiel AM, Duyckaerts C, Javoy-Agid F. Neuronal loss in the pedunculopontine tegmental nucleus in Parkinson disease and in progressive supranuclear palsy. Proc Natl Acad Sci U S A. 1987;84(16):5976–80.CrossRefGoogle Scholar
  19. 19.
    Jellinger K. The pedunculopontine nucleus in Parkinson’s disease, progressive supranuclear palsy and Alzheimer’s disease. J Neurol Neurosurg Psychiatry. 1988;51(4):540–3.CrossRefGoogle Scholar
  20. 20.
    Zweig RM, Jankel WR, Hedreen JC, Mayeux R, Price DL. The pedunculopontine nucleus in Parkinson’s disease. Ann Neurol. 1989;26(1):41–6.CrossRefGoogle Scholar
  21. 21.
    Karachi C, Grabli D, Bernard FA, Tande D, Wattiez N, Belaid H, et al. Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J Clin Invest. 2010;120(8):2745–54.CrossRefGoogle Scholar
  22. 22.
    Grabli D, Karachi C, Folgoas E, Monfort M, Tande D, Clark S, et al. Gait disorders in parkinsonian monkeys with pedunculopontine nucleus lesions: a tale of two systems. J Neurosci. 2013;33(29):11986–93.CrossRefGoogle Scholar
  23. 23.
    Postuma RB, Gagnon JF, Bertrand JA, Genier Marchand D, Montplaisir JY. Parkinson risk in idiopathic REM sleep behavior disorder: preparing for neuroprotective trials. Neurology. 2015;84(11):1104–13.CrossRefGoogle Scholar
  24. 24.
    Postuma RB, Lang AE, Massicotte-Marquez J, Montplaisir J. Potential early markers of Parkinson disease in idiopathic REM sleep behavior disorder. Neurology. 2006;66(6):845–51.CrossRefGoogle Scholar
  25. 25.
    Potter-Nerger M, Volkmann J. Deep brain stimulation for gait and postural symptoms in Parkinson’s disease. Mov Disord. 2013;28(11):1609–15.CrossRefGoogle Scholar
  26. 26.
    Wan Y, Luo Y, Gan J, Hu R, Zhou M, Liu Z. Clinical markers of neurodegeneration in Chinese patients with idiopathic rapid eye movement sleep behavior disorder. Clin Neurol Neurosurg. 2016;150:105–9.CrossRefGoogle Scholar
  27. 27.
    Alibiglou L, Videnovic A, Planetta PJ, Vaillancourt DE, MacKinnon CD. Subliminal gait initiation deficits in rapid eye movement sleep behavior disorder: a harbinger of freezing of gait? Mov Disord. 2016;31(11):1711–9.CrossRefGoogle Scholar
  28. 28.
    Burleigh-Jacobs A, Horak FB, Nutt JG, Obeso JA. Step initiation in Parkinson’s disease: influence of levodopa and external sensory triggers. Mov Disord. 1997;12(2):206–15.CrossRefGoogle Scholar
  29. 29.
    Rogers MW, Kennedy R, Palmer S, Pawar M, Reising M, Martinez KM, et al. Postural preparation prior to stepping in patients with Parkinson’s disease. J Neurophysiol. 2011;106(2):915–24.CrossRefGoogle Scholar
  30. 30.
    Delval A, Tard C, Defebvre L. Why we should study gait initiation in Parkinson’s disease. Clin Neurophysiol. 2014;44(1):69–76.CrossRefGoogle Scholar
  31. 31.
    Hallett M, Khoshbin S. A physiological mechanism of bradykinesia. Brain. 1980;103(2):301–14.CrossRefGoogle Scholar
  32. 32.
    Pfann KD, Buchman AS, Comella CL, Corcos DM. Control of movement distance in Parkinson’s disease. Mov Disord. 2001;16(6):1048–65.CrossRefGoogle Scholar
  33. 33.
    Robichaud JA, Pfann KD, Comella CL, Corcos DM. Effect of medication on EMG patterns in individuals with Parkinson’s disease. Mov Disord. 2002;17(5):950–60.CrossRefGoogle Scholar
  34. 34.
    Robichaud JA, Pfann KD, Leurgans S, Vaillancourt DE, Comella CL, Corcos DM. Variability of EMG patterns: a potential neurophysiological marker of Parkinson’s disease? Clin Neurophysiol. 2009;120(2):390–7.CrossRefGoogle Scholar
  35. 35.
    Freund HJ. Motor unit and muscle activity in voluntary motor control. Physiol Rev. 1983;63(2):387–436.CrossRefGoogle Scholar
  36. 36.
    Dietz V, Hillesheimer W, Freund HJ. Correlation between tremor, voluntary contraction, and firing pattern of motor units in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1974;37(8):927–37.CrossRefGoogle Scholar
  37. 37.
    Dengler R, Wolf W, Schubert M, Struppler A. Discharge pattern of single motor units in basal ganglia disorders. Neurology. 1986;36(8):1061–6.CrossRefGoogle Scholar
  38. 38.
    Wilson jM, Thompson CK, Miller LC, MacKinnon CD, Heckman CJ, editors. Paradoxical changes in intrinsic motoneuron excitability between flexors and extensors in Parkinson’s disease. Chicago: Society for Neuroscience; 2015.Google Scholar
  39. 39.
    Holstege JC, Kuypers HG. Brainstem projections to lumbar motoneurons in rat–I. An ultrastructural study using autoradiography and the combination of autoradiography and horseradish peroxidase histochemistry. Neuroscience. 1987;21(2):345–67.CrossRefGoogle Scholar
  40. 40.
    Hornung JP. The human raphe nuclei and the serotonergic system. J Chem Neuroanat. 2003;26(4):331–43.CrossRefGoogle Scholar
  41. 41.
    Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J. Motoneuron excitability: the importance of neuromodulatory inputs. Clin Neurophysiol. 2009;120(12):2040–54.CrossRefGoogle Scholar
  42. 42.
    Postuma RB, Gagnon JF, Vendette M, Charland K, Montplaisir J. REM sleep behaviour disorder in Parkinson’s disease is associated with specific motor features. J Neurol Neurosurg Psychiatry. 2008;79(10):1117–21.CrossRefGoogle Scholar
  43. 43.
    Bugalho P, Viana-Baptista M. REM sleep behavior disorder and motor dysfunction in Parkinson’s disease–a longitudinal study. Parkinsonism Relat Disord. 2013;19(12):1084–7.CrossRefGoogle Scholar
  44. 44.
    Kang SH, Lee HM, Seo WK, Kim JH, Koh SB. The combined effect of REM sleep behavior disorder and hyposmia on cognition and motor phenotype in Parkinson’s disease. J Neurol Sci. 2016;368:374–8.CrossRefGoogle Scholar
  45. 45.
    Romenets SR, Gagnon JF, Latreille V, Panniset M, Chouinard S, Montplaisir J, et al. Rapid eye movement sleep behavior disorder and subtypes of Parkinson’s disease. Mov Disord. 2012;27(8):996–1003.CrossRefGoogle Scholar
  46. 46.
    Videnovic A, Marlin C, Alibiglou L, Planetta PJ, Vaillancourt DE, Mackinnon CD. Increased REM sleep without atonia in Parkinson disease with freezing of gait. Neurology. 2013;81(12):1030–5.CrossRefGoogle Scholar
  47. 47.
    Benninger DH, Michel J, Waldvogel D, Candia V, Poryazova R, van Hedel HJ, et al. REM sleep behavior disorder is not linked to postural instability and gait dysfunction in Parkinson. Mov Disord. 2010;25(11):1597–604.CrossRefGoogle Scholar
  48. 48.
    Curtze C, Nutt JG, Carlson-Kuhta P, Mancini M, Horak FB. Levodopa is a double-edged sword for balance and gait in people with Parkinson’s disease. Mov Disord. 2015;30(10):1361–70.CrossRefGoogle Scholar
  49. 49.
    Kotagal V, Albin RL, Muller ML, Koeppe RA, Chervin RD, Frey KA, et al. Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann Neurol. 2012;71(4):560–8.CrossRefGoogle Scholar
  50. 50.
    Bohnen NI, Muller ML, Koeppe RA, Studenski SA, Kilbourn MA, Frey KA, et al. History of falls in Parkinson disease is associated with reduced cholinergic activity. Neurology. 2009;73(20):1670–6.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2019

Authors and Affiliations

  • Colum D. MacKinnon
    • 1
    • 2
    Email author
  • Laila Alibiglou
    • 3
    • 4
  • Aleksandar Videnovic
    • 5
  1. 1.Department of NeurologyUniversity of MinnesotaMinneapolisUSA
  2. 2.Institute of Translational Neuroscience, University of MinnesotaMinneapolisUSA
  3. 3.Department of Physical TherapyRosalind Franklin University of Medicine and ScienceNorth ChicagoUSA
  4. 4.Department of NeuroscienceRosalind Franklin University of Medicine and ScienceNorth ChicagoUSA
  5. 5.Department of NeurologyMassachusetts General Hospital, Harvard Medical SchoolBostonUSA

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