Balance control systems in Parkinson’s disease and the impact of pedunculopontine area stimulation

See Xiang et al. (doi:10.1093/brain/awy250) for a scientific commentary on this article. Balance impairment in Parkinson's disease decreases quality of life and is often refractory to treatment. Perera et al. report that balance impairment relates to deficits in intermittent and continuous control systems proposed to maintain upright stance. The deficits may be reversible with the experimental therapy, pedunculopontine nucleus deep brain stimulation.

[1]  Ian Loram,et al.  Wavelet-frequency analysis for the detection of discontinuities in switched system models of human balance. , 2017, Human movement science.

[2]  J. H. J. Allum,et al.  Subthalamic nucleus stimulation and levodopa-resistant postural instability in Parkinson's disease , 2008, Journal of Neurology.

[3]  Mandy Miller Koop,et al.  Excessive postural sway and the risk of falls at different stages of Parkinson's disease , 2009, Movement disorders : official journal of the Movement Disorder Society.

[4]  H. Straka,et al.  Postural Control: Learning to Balance Is a Question of Timing , 2017, Current Biology.

[5]  James R. Chagdes,et al.  The relationship between intermittent limit cycles and postural instability associated with Parkinson's disease , 2016, Journal of sport and health science.

[6]  Taishin Nomura,et al.  Bounded stability of the quiet standing posture: an intermittent control model. , 2008, Human movement science.

[7]  P. Brown,et al.  A block to pre-prepared movement in gait freezing, relieved by pedunculopontine nucleus stimulation , 2011, Brain : a journal of neurology.

[8]  Alpha oscillations in the pedunculopontine nucleus correlate with gait performance in parkinsonism , 2012, Brain : a journal of neurology.

[9]  Natalie E. Allen,et al.  Postural Instability in Patients with Parkinson’s Disease , 2013, CNS Drugs.

[10]  Richard M. Murray,et al.  Feedback Systems An Introduction for Scientists and Engineers , 2007 .

[11]  M. Hallett,et al.  Physiology of freezing of gait , 2016, Annals of neurology.

[12]  S Fahn,et al.  Freezing of gait in PD , 2001, Neurology.

[13]  Francesco Pierelli,et al.  Balance Dysfunction in Parkinson's Disease , 2015, BioMed research international.

[14]  Taishin Nomura,et al.  A Classification of Postural Sway Patterns During Upright Stance in Healthy Adults and Patients with Parkinson's Disease , 2011, J. Adv. Comput. Intell. Intell. Informatics.

[15]  P. Brown,et al.  The impact of low-frequency stimulation of the pedunculopontine nucleus region on reaction time in parkinsonism , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[16]  M. Hely,et al.  The Sydney multicentre study of Parkinson’s disease: progression and mortality at 10 years , 1999, Journal of neurology, neurosurgery, and psychiatry.

[17]  Peter J. Gawthrop,et al.  Intermittent control models of human standing: similarities and differences , 2014, Biological Cybernetics.

[18]  P. Sah,et al.  Imagined gait modulates neuronal network dynamics in the human pedunculopontine nucleus , 2014, Nature Neuroscience.

[19]  P. Bain,et al.  The effect of pedunculopontine nucleus deep brain stimulation on postural sway and vestibular perception , 2016, European journal of neurology.

[20]  J. Duysens,et al.  The effects of an auditory startle on obstacle avoidance during walking , 2008, The Journal of physiology.

[21]  F. Horak,et al.  Postural inflexibility in parkinsonian subjects , 1992, Journal of the Neurological Sciences.

[22]  J. Valls-Solé,et al.  Interaction between startle and voluntary reactions in humans , 2008, Experimental Brain Research.

[23]  Hayat Belaid,et al.  PPNa-DBS for gait and balance disorders in Parkinson’s disease: a double-blind, randomised study , 2015, Journal of Neurology.

[24]  J. Salamone,et al.  Paradoxical kinesia in parkinsonism is not caused by dopamine release. Studies in an animal model. , 1989, Archives of neurology.

[25]  S. Factor,et al.  The clinical spectrum of freezing of gait in atypical parkinsonism , 2008, Movement disorders : official journal of the Movement Disorder Society.

[26]  G. Naglie,et al.  Predictors of deterioration in health‐related quality of life in Parkinson's disease: Results from the DATATOP trial , 2008, Movement disorders : official journal of the Movement Disorder Society.

[27]  Tipu Aziz,et al.  Pedunculopontine nucleus deep brain stimulation in Parkinson's disease: A clinical review , 2018, Movement disorders : official journal of the Movement Disorder Society.

[28]  Francesco Rea,et al.  Stabilization strategies for unstable dynamics. , 2014, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[29]  Jeffrey M. Hausdorff,et al.  Falls and freezing of gait in Parkinson's disease: A review of two interconnected, episodic phenomena , 2004, Movement disorders : official journal of the Movement Disorder Society.

[30]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. II. The effects of lesions of the descending brain-stem pathways. , 1968, Brain : a journal of neurology.

[31]  S Fahn,et al.  Evaluation of the pull test technique in assessing postural instability in Parkinson’s disease , 2004, Neurology.

[32]  P. Bauer,et al.  Screening of mutations in GNAL in sporadic dystonia patients , 2014, Movement disorders : official journal of the Movement Disorder Society.

[33]  Tipu Z. Aziz,et al.  A spatiotemporal analysis of gait freezing and the impact of pedunculopontine nucleus stimulation , 2012, Brain : a journal of neurology.

[34]  M M Mesulam,et al.  Human reticular formation: Cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons , 1989, The Journal of comparative neurology.

[35]  V. Weerdesteyn,et al.  StartReact Effects Support Different Pathophysiological Mechanisms Underlying Freezing of Gait and Postural Instability in Parkinson’s Disease , 2015, PloS one.

[36]  J. Valls-Solé,et al.  Reaction time and acoustic startle in normal human subjects , 1995, Neuroscience Letters.

[37]  K. Hidenori,et al.  A PID model of human balance keeping , 2006, IEEE Control Systems.

[38]  Claudia D. Jarrin Tejada,et al.  Effect of Dopaminergic Medication on Postural Sway in Advanced Parkinson’s Disease , 2013, Front. Neurol..

[39]  E. Heremans,et al.  Clinical balance scales indicate worse postural control in people with Parkinson's disease who exhibit freezing of gait compared to those who do not: A meta-analysis. , 2017, Gait & posture.

[40]  F. Grandas,et al.  Effect of subthalamic nucleus deep brain stimulation on balance in Parkinson's disease: A static posturographic analysis. , 2017, Gait & posture.

[41]  T. Mergner,et al.  Abnormal resonance behavior of the postural control loop in Parkinson’s disease , 2004, Experimental Brain Research.

[42]  Clement Hamani,et al.  Pedunculopontine Nucleus Region Deep Brain Stimulation in Parkinson Disease: Surgical Techniques, Side Effects, and Postoperative Imaging , 2016, Stereotactic and Functional Neurosurgery.

[43]  Anand I. Rughani,et al.  Pedunculopontine Nucleus Region Deep Brain Stimulation in Parkinson Disease: Surgical Anatomy and Terminology , 2016, Stereotactic and Functional Neurosurgery.

[44]  Nir Giladi,et al.  Construction of freezing of gait questionnaire for patients with Parkinsonism. , 2000, Parkinsonism & related disorders.

[45]  Peter J. Gawthrop,et al.  Intermittent control: a computational theory of human control , 2011, Biological Cybernetics.

[46]  Houeto Jean-Luc.  [Parkinson's disease]. , 2022, La Revue du praticien.

[47]  D. German,et al.  Quantification of cholinergic and select non-cholinergic mesopontine neuronal populations in the human brain , 1999, Neuroscience.

[48]  Bastiaan R. Bloem,et al.  Measurement instruments to assess posture, gait, and balance in Parkinson's disease: Critique and recommendations , 2016, Movement disorders : official journal of the Movement Disorder Society.

[49]  R. Peterka.  Sensorimotor integration in human postural control. , 2002, Journal of neurophysiology.

[50]  Ian M Franks,et al.  Precues enable multiple response preprogramming: evidence from startle. , 2009, Psychophysiology.

[51]  Boualem Boashash,et al.  Estimating and interpreting the instantaneous frequency of a signal. I. Fundamentals , 1992, Proc. IEEE.

[52]  Henrik Gollee,et al.  Human control of an inverted pendulum: Is continuous control necessary? Is intermittent control effective? Is intermittent control physiological? , 2011, The Journal of physiology.

[53]  Martina Mancini,et al.  Framework for understanding balance dysfunction in Parkinson's disease , 2013, Movement disorders : official journal of the Movement Disorder Society.

[54]  Nicola J. Ray,et al.  Anatomy, physiology, and pathophysiology of the pedunculopontine nucleus , 2009, Movement disorders : official journal of the Movement Disorder Society.

[55]  Robert A Koeppe,et al.  Thalamic cholinergic innervation and postural sensory integration function in Parkinson's disease. , 2013, Brain : a journal of neurology.

[56]  G. Thickbroom,et al.  Clinical and posturographic correlates of falling in Parkinson's disease , 2013, Movement disorders : official journal of the Movement Disorder Society.

[57]  Raija Korpelainen,et al.  Postural sway and falls in Parkinson's disease: A regression approach , 2007, Movement disorders : official journal of the Movement Disorder Society.

[58]  T. Aziz,et al.  Deep brain stimulation of the pedunculopontine nucleus in Parkinson's disease. Preliminary experience at Oxford , 2008, British journal of neurosurgery.

[59]  Ned Jenkinson,et al.  Pedunculopontine Nucleus Stimulation Improves Gait Freezing in Parkinson Disease , 2011, Neurosurgery.

[60]  J. Jankovic.  Parkinson’s disease: clinical features and diagnosis , 2008, Journal of Neurology, Neurosurgery, and Psychiatry.

[61]  Clement Hamani,et al.  Unilateral pedunculopontine stimulation improves falls in Parkinson's disease. , 2010, Brain : a journal of neurology.

[62]  Milos R Popovic,et al.  Controlling balance during quiet standing: proportional and derivative controller generates preceding motor command to body sway position observed in experiments. , 2006, Gait & posture.

[63]  B. R. Bloem,et al.  Are postural responses to backward and forward perturbations processed by different neural circuits? , 2013, Neuroscience.

[64]  M. Glickstein,et al.  Paradoxical movement in Parkinson's disease , 1991, Trends in Neurosciences.

[65]  A. Lieberman,et al.  Parkinson's disease: a clinical review. , 1974, The American journal of the medical sciences.

[66]  Robert J. Peterka,et al.  Postural control model interpretation of stabilogram diffusion analysis , 2000, Biological Cybernetics.

[67]  A. Benabid,et al.  Pedunculopontine Nucleus Area Oscillations during Stance, Stepping and Freezing in Parkinson’s Disease , 2013, PloS one.

[68]  B. Lau,et al.  The integrative role of the pedunculopontine nucleus in human gait. , 2015, Brain : a journal of neurology.

[69]  C H Lücking,et al.  Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson's disease. , 2003, Brain : a journal of neurology.

[70]  D. Winter,et al.  Assessment of balance control in humans. , 1990, Medical progress through technology.

[71]  P. Mosterman,et al.  A theory of discontinuities in physical system models , 1998 .

[72]  Anthony N. Carlsen,et al.  Differential effects of startle on reaction time for finger and arm movements. , 2009, Journal of neurophysiology.

[73]  G. Ebersbach,et al.  Posturography reflects clinical imbalance in Parkinson's disease , 2011, Movement disorders : official journal of the Movement Disorder Society.

[74]  C. MacKinnon,et al.  Preparation of anticipatory postural adjustments prior to stepping. , 2007, Journal of neurophysiology.

[75]  Motoki Kouzaki,et al.  Effect of intermittent feedback control on robustness of human-like postural control system , 2016, Scientific Reports.

[76]  G. Kwakkel,et al.  Cueing training in the home improves gait-related mobility in Parkinson’s disease: the RESCUE trial , 2007, Journal of Neurology, Neurosurgery & Psychiatry.

[77]  S. Rehncrona,et al.  Multicenter study on deep brain stimulation in Parkinson's disease: An independent assessment of reported adverse events at 4 years , 2008, Movement disorders : official journal of the Movement Disorder Society.

[78]  E. Tolosa,et al.  Validation of the freezing of gait questionnaire in patients with Parkinson's disease , 2009, Movement disorders : official journal of the Movement Disorder Society.

[79]  P. Morasso,et al.  Body sway during quiet standing: is it the residual chattering of an intermittent stabilization process? , 2005, Human movement science.

[80]  V. Preedy,et al.  Unified Parkinson's Disease Rating Scale , 2010 .

[81]  V. Weerdesteyn,et al.  Reduced StartReact effect and freezing of gait in Parkinson’s disease: two of a kind? , 2014, Journal of Neurology.

[82]  B Piallat,et al.  Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson's disease. , 2010, Brain : a journal of neurology.

[83]  J. Rothwell,et al.  Patterned ballistic movements triggered by a startle in healthy humans , 1999, The Journal of physiology.

[84]  Angelo Cappello,et al.  Identification of distinct characteristics of postural sway in Parkinson's disease: A feature selection procedure based on principal component analysis , 2006, Neuroscience Letters.

[85]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[86]  A. Bonnet,et al.  [The Unified Parkinson's Disease Rating Scale]. , 2000, Revue neurologique.

[87]  F. Horak,et al.  A meta-regression of the long-term effects of deep brain stimulation on balance and gait in PD , 2010, Neurology.

[88]  Nir Giladi,et al.  Gait festination in Parkinson's disease. , 2001, Parkinsonism & related disorders.