Semin Neurol 2017; 37(02): 109-117
DOI: 10.1055/s-0037-1601869
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

The Phenomenology of Parkinson's Disease

Christopher W. Hess
1   Department of Neurology, University of Florida, Center for Movement Disorders and Neurorestoration, Gainesville, Florida
,
Mark Hallett
2   Human Motor Control Section, Medical Neurology Branch, NINDS, NIH, Bethesda, Maryland
› Author Affiliations
Further Information

Publication History

Publication Date:
16 May 2017 (online)

Abstract

The motor symptoms of Parkinson's disease are not limited to the cardinal symptoms of bradykinesia, rigidity, and resting tremor, but also include a variety of interrelated motor phenomena such as deficits in spatiotemporal planning and movement sequencing, scaling and timing of movements, and intermuscular coordination that can be clinically observed. Although many of these phenomena overlap, a review of the full breadth of the motor phenomenon can aid in the diagnosis and monitoring of disease progression.

 
  • References

  • 1 Frucht SJ, Fahn S. Movement Disorder Emergencies: Diagnosis and Treatment. Totowa, NJ: Humana Press; 2005
  • 2 Kim YE, Jeon BS. Musculoskeletal problems in Parkinson's disease. J Neural Transm (Vienna) 2013; 120 (4) 537-542
  • 3 Stocchi F, Barbato L, Nordera G, Berardelli A, Ruggieri S. Sleep disorders in Parkinson's disease. J Neurol 1998; 245 (Suppl. 01) S15-S18
  • 4 Fahn S, Jankovic J, Hallett M. Principles and practice of movement disorders. 2nd ed. Philadelphia, PA: Elsevier/Saunders; 2011
  • 5 Giladi N, McMahon D, Przedborski S , et al. Motor blocks in Parkinson's disease. Neurology 1992; 42 (2) 333-339
  • 6 Hallett M. The intrinsic and extrinsic aspects of freezing of gait. Mov Disord 2008; 23 (Suppl. 02) S439-S443
  • 7 Wong AL, Haith AM, Krakauer JW. Motor planning. Neuroscientist 2015; 21 (4) 385-398
  • 8 Kutukcu Y, Marks Jr WJ, Goodin DS, Aminoff MJ. Simple and choice reaction time in Parkinson's disease. Brain Res 1999; 815 (2) 367-372
  • 9 Berardelli A, Rothwell JC, Thompson PD, Hallett M. Pathophysiology of bradykinesia in Parkinson's disease. Brain 2001; 124 (Pt 11): 2131-2146
  • 10 Carlsen AN, Almeida QJ, Franks IM. Using a startling acoustic stimulus to investigate underlying mechanisms of bradykinesia in Parkinson's disease. Neuropsychologia 2013; 51 (3) 392-399
  • 11 Hallett M, Shahani BT, Young RR. Analysis of stereotyped voluntary movements at the elbow in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 1977; 40 (12) 1129-1135
  • 12 Macerollo A, Chen JC, Korlipara P , et al. Dopaminergic treatment modulates sensory attenuation at the onset of the movement in Parkinson's disease: a test of a new framework for bradykinesia. Mov Disord 2016; 31 (1) 143-146
  • 13 Mazzoni P, Shabbott B, Cortés JC. Motor control abnormalities in Parkinson's disease. Cold Spring Harb Perspect Med 2012; 2 (6) a009282
  • 14 Hess CW, Okun MS. Diagnosing Parkinson disease. Continuum (Minneap Minn) 2016; 22 (4 Movement Disorders): 1047-1063
  • 15 Hallett M, Khoshbin S. A physiological mechanism of bradykinesia. Brain 1980; 103 (2) 301-314
  • 16 Benecke R, Rothwell JC, Dick JP, Day BL, Marsden CD. Simple and complex movements off and on treatment in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 1987; 50 (3) 296-303
  • 17 Hallett M. Bradykinesia: why do Parkinson's patients have it and what trouble does it cause?. Mov Disord 2011; 26 (9) 1579-1581
  • 18 Mazzoni P, Hristova A, Krakauer JW. Why don't we move faster? Parkinson's disease, movement vigor, and implicit motivation. J Neurosci 2007; 27 (27) 7105-7116
  • 19 Baraduc P, Thobois S, Gan J, Broussolle E, Desmurget M. A common optimization principle for motor execution in healthy subjects and parkinsonian patients. J Neurosci 2013; 33 (2) 665-677
  • 20 Demirci M, Grill S, McShane L, Hallett M. A mismatch between kinesthetic and visual perception in Parkinson's disease. Ann Neurol 1997; 41 (6) 781-788
  • 21 Tinaz S, Pillai AS, Hallett M. sequence effect in Parkinson's disease is related to motor energetic cost. Front Neurol 2016; 7: 83
  • 22 van Hilten JJ, van Eerd AA, Wagemans EA, Middelkoop HA, Roos RA. Bradykinesia and hypokinesia in Parkinson's disease: what's in a name?. J Neural Transm (Vienna) 1998; 105 (2-3): 229-237
  • 23 Chaudhuri A, Behan PO. Fatigue and basal ganglia. J Neurol Sci 2000; 179 (S 1-2): 34-42
  • 24 Oliveira RM, Gurd JM, Nixon P, Marshall JC, Passingham RE. Micrographia in Parkinson's disease: the effect of providing external cues. J Neurol Neurosurg Psychiatry 1997; 63 (4) 429-433
  • 25 Wu T, Zhang J, Hallett M, Feng T, Hou Y, Chan P. Neural correlates underlying micrographia in Parkinson's disease. Brain 2016; 139 (Pt 1): 144-160
  • 26 Ling H, Massey LA, Lees AJ, Brown P, Day BL. Hypokinesia without decrement distinguishes progressive supranuclear palsy from Parkinson's disease. Brain 2012; 135 (Pt 4): 1141-1153
  • 27 Kang SY, Wasaka T, Shamim EA , et al. The sequence effect in de novo Parkinson's disease. J Mov Disord 2011; 4 (1) 38-40
  • 28 Kang SY, Wasaka T, Shamim EA , et al. Characteristics of the sequence effect in Parkinson's disease. Mov Disord 2010; 25 (13) 2148-2155
  • 29 Berardelli A, Wenning GK, Antonini A , et al. EFNS/MDS-ES/ENS [corrected] recommendations for the diagnosis of Parkinson's disease. Eur J Neurol 2013; 20 (1) 16-34
  • 30 Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992; 55 (3) 181-184
  • 31 Allen NE, Canning CG, Sherrington C, Fung VS. Bradykinesia, muscle weakness and reduced muscle power in Parkinson's disease. Mov Disord 2009; 24 (9) 1344-1351
  • 32 Park JH, Stelmach GE. Force development during target-directed isometric force production in Parkinson's disease. Neurosci Lett 2007; 412 (2) 173-178
  • 33 Corcos DM, Chen CM, Quinn NP, McAuley J, Rothwell JC. Strength in Parkinson's disease: relationship to rate of force generation and clinical status. Ann Neurol 1996; 39 (1) 79-88
  • 34 Friedman JH, Abrantes AM. Self perceived weakness in Parkinson's disease. Parkinsonism Relat Disord 2012; 18 (7) 887-889
  • 35 Brown P, Corcos DM, Rothwell JC. Does parkinsonian action tremor contribute to muscle weakness in Parkinson's disease?. Brain 1997; 120 (Pt 3): 401-408
  • 36 Powell D, Muthumani A, Xia R. A comparison of the effects of continuous versus discontinuous movement patterns on parkinsonian rigidity and reflex responses to passive stretch and shortening. J Nat Sci 2016; 2 (8) e201
  • 37 Xia R, Powell D, Rymer WZ, Hanson N, Fang X, Threlkeld AJ. Differentiation between the contributions of shortening reaction and stretch-induced inhibition to rigidity in Parkinson's disease. Exp Brain Res 2011; 209 (4) 609-618
  • 38 Broussolle E, Krack P, Thobois S, Xie-Brustolin J, Pollak P, Goetz CG. Contribution of Jules Froment to the study of parkinsonian rigidity. Mov Disord 2007; 22 (7) 909-914
  • 39 Prochazka A, Bennett DJ, Stephens MJ , et al. Measurement of rigidity in Parkinson's disease. Mov Disord 1997; 12 (1) 24-32
  • 40 Abdolahi A, Scoglio N, Killoran A, Dorsey ER, Biglan KM. Potential reliability and validity of a modified version of the Unified Parkinson's Disease Rating Scale that could be administered remotely. Parkinsonism Relat Disord 2013; 19 (2) 218-221
  • 41 Berardelli A, Sabra AF, Hallett M. Physiological mechanisms of rigidity in Parkinson's disease. J Neurol Neurosurg Psychiatry 1983; 46 (1) 45-53
  • 42 Xia R, Muthumani A, Mao ZH, Powell DW. Quantification of neural reflex and muscular intrinsic contributions to parkinsonian rigidity. Exp Brain Res 2016; 234 (12) 3587-3595
  • 43 Pasquereau B, Turner RS. Primary motor cortex of the parkinsonian monkey: altered neuronal responses to muscle stretch. Front Syst Neurosci 2013; 7: 98
  • 44 Raoul S, Roualdes V, Deligny C , et al. Subthalamic nucleus stimulation reverses spinal motoneuron activity in parkinsonian patients. Brain 2012; 135 (Pt 1): 139-147
  • 45 Kwon KY, Kim M, Lee SM, Kang SH, Lee HM, Koh SB. Is reduced arm and leg swing in Parkinson's disease associated with rigidity or bradykinesia?. J Neurol Sci 2014; 341 (1-2): 32-35
  • 46 Meyns P, Bruijn SM, Duysens J. The how and why of arm swing during human walking. Gait Posture 2013; 38 (4) 555-562
  • 47 Wu T, Hallett M. The influence of normal human ageing on automatic movements. J Physiol 2005; 562 (Pt 2): 605-615
  • 48 Marsden CD. The mysterious motor function of the basal ganglia: the Robert Wartenberg Lecture. Neurology 1982; 32 (5) 514-539
  • 49 Wu T, Hallett M, Chan P. Motor automaticity in Parkinson's disease. Neurobiol Dis 2015; 82: 226-234
  • 50 Wu T, Wang L, Hallett M, Li K, Chan P. Neural correlates of bimanual anti-phase and in-phase movements in Parkinson's disease. Brain 2010; 133 (Pt 8): 2394-2409
  • 51 Johnson KA, Cunnington R, Bradshaw JL, Phillips JG, Iansek R, Rogers MA. Bimanual co-ordination in Parkinson's disease. Brain 1998; 121 (Pt 4): 743-753
  • 52 Espay AJ, Li JY, Johnston L, Chen R, Lang AE. Mirror movements in parkinsonism: evaluation of a new clinical sign. J Neurol Neurosurg Psychiatry 2005; 76 (10) 1355-1358
  • 53 Cox BC, Cincotta M, Espay AJ. Mirror movements in movement disorders: a review. Tremor Other Hyperkinet Mov (N Y) 2012; 2: 2
  • 54 Artieda J, Pastor MA, Lacruz F, Obeso JA. Temporal discrimination is abnormal in Parkinson's disease. Brain 1992; 115 (Pt 1): 199-210
  • 55 Pastor MA, Artieda J, Jahanshahi M, Obeso JA. Time estimation and reproduction is abnormal in Parkinson's disease. Brain 1992; 115 (Pt 1): 211-225
  • 56 Trager MH, Velisar A, Koop MM, Shreve L, Quinn E, Bronte-Stewart H. Arrhythmokinesis is evident during unimanual not bimanual finger tapping in Parkinson's disease. J Clin Mov Disord 2015; 2: 8
  • 57 Brown RG, Marsden CD. Internal versus external cues and the control of attention in Parkinson's disease. Brain 1988; 111 (Pt 2): 323-345
  • 58 Sarma SV, Cheng ML, Eden U, Williams Z, Brown EN, Eskandar E. The effects of cues on neurons in the basal ganglia in Parkinson's disease. Front Integr Nuerosci 2012; 6: 40
  • 59 Flowers K. Lack of prediction in the motor behaviour of parkinsonism. Brain 1978; 101 (1) 35-52
  • 60 Currà A, Berardelli A, Agostino R , et al. Performance of sequential arm movements with and without advance knowledge of motor pathways in Parkinson's disease. Mov Disord 1997; 12 (5) 646-654
  • 61 Michely J, Volz LJ, Barbe MT , et al. Dopaminergic modulation of motor network dynamics in Parkinson's disease. Brain 2015; 138 (Pt 3): 664-678
  • 62 Nieuwboer A, Baker K, Willems AM , et al. The short-term effects of different cueing modalities on turn speed in people with Parkinson's disease. Neurorehabil Neural Repair 2009; 23 (8) 831-836
  • 63 Jankovic J. Parkinson's disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 2008; 79 (4) 368-376
  • 64 Souques A. Kinésie paradoxale. Rev Neurol 1921; 37: 559-560
  • 65 Schlesinger I, Erikh I, Yarnitsky D. Paradoxical kinesia at war. Mov Disord 2007; 22 (16) 2394-2397
  • 66 Daroff RB. Paradoxical kinesia. Mov Disord 2008; 23 (8) 1193
  • 67 McDonald LM, Griffin HJ, Angeli A, Torkamani M, Georgiev D, Jahanshahi M. Motivational modulation of self-initiated and externally triggered movement speed induced by threat of shock: experimental evidence for paradoxical kinesis in Parkinson's disease. PLoS One 2015; 10 (8) e0135149
  • 68 Robottom BJ, Weiner WJ, Asmus F, Huber H, Gasser T, Schöls L. Kick and rush: paradoxical kinesia in Parkinson disease. Neurology 2009; 73 (4) 328 , author reply 328–329
  • 69 Bonanni L, Thomas A, Anzellotti F , et al. Protracted benefit from paradoxical kinesia in typical and atypical parkinsonisms. Neurol Sci 2010; 31 (6) 751-756
  • 70 Anzak A, Tan H, Pogosyan A , et al. Subcortical evoked activity and motor enhancement in Parkinson's disease. Exp Neurol 2016; 277: 19-26
  • 71 Parkinson J. An essay on the shaking palsy. 1817. J Neuropsychiatry Clin Neurosci 2002; 14 (2) 223-236 , discussion 222
  • 72 Giladi N, Shabtai H, Rozenberg E, Shabtai E. Gait festination in Parkinson's disease. Parkinsonism Relat Disord 2001; 7 (2) 135-138
  • 73 Rossi M, Cerquetti D, Merello M. Piano playing festination as initial symptom of Parkinson's disease. Parkinsonism Relat Disord 2015; 21 (4) 417-418
  • 74 Moreau C, Ozsancak C, Blatt JL, Derambure P, Destee A, Defebvre L. Oral festination in Parkinson's disease: biomechanical analysis and correlation with festination and freezing of gait. Mov Disord 2007; 22 (10) 1503-1506
  • 75 Starkstein S, Dragovic M, Brockman S, Wilson M, Bruno V, Merello M. The impact of emotional distress on motor blocks and festination in Parkinson's disease. J Neuropsychiatry Clin Neurosci 2015; 27 (2) 121-126
  • 76 Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 2011; 10 (8) 734-744
  • 77 Schaafsma JD, Balash Y, Gurevich T, Bartels AL, Hausdorff JM, Giladi N. Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson's disease. Eur J Neurol 2003; 10 (4) 391-398
  • 78 Snijders AH, Takakusaki K, Debu B , et al. Physiology of freezing of gait. Ann Neurol 2016; 80 (5) 644-659
  • 79 Heremans E, Nackaerts E, Vervoort G , et al. Amplitude manipulation evokes upper limb freezing during handwriting in patients with Parkinson's disease with freezing of gait. PLoS One 2015; 10 (11) e0142874
  • 80 Vercruysse S, Gilat M, Shine JM, Heremans E, Lewis S, Nieuwboer A. Freezing beyond gait in Parkinson's disease: a review of current neurobehavioral evidence. Neurosci Biobehav Rev 2014; 43: 213-227
  • 81 Ziv I, Avraham M, Dabby R, Zoldan J, Djaldetti R, Melamed E. Early-occurrence of manual motor blocks in Parkinson's disease: a quantitative assessment. Acta Neurol Scand 1999; 99 (2) 106-111
  • 82 Iansek R, Huxham F, McGinley J. The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait?. Mov Disord 2006; 21 (9) 1419-1424
  • 83 Rahman S, Griffin HJ, Quinn NP, Jahanshahi M. On the nature of fear of falling in Parkinson's disease. Behav Neurol 2011; 24 (3) 219-228
  • 84 Agostino R, Currà A, Giovannelli M, Modugno N, Manfredi M, Berardelli A. Impairment of individual finger movements in Parkinson's disease. Mov Disord 2003; 18 (5) 560-565
  • 85 Heilman KM. Apraxia. Continuum (Minneap Minn) 2010; 16 (4 Behavioral Neurology): 86-98
  • 86 Pearce JM. Hugo Karl Liepmann and apraxia. Clin Med (Lond) 2009; 9 (5) 466-470
  • 87 Leiguarda RC, Marsden CD. Limb apraxias: higher-order disorders of sensorimotor integration. Brain 2000; 123 (Pt 5): 860-879
  • 88 Pramstaller PP, Marsden CD. The basal ganglia and apraxia. Brain 1996; 119 (Pt 1): 319-340
  • 89 Heilman KM, Meador KJ, Loring DW. Hemispheric asymmetries of limb-kinetic apraxia: a loss of deftness. Neurology 2000; 55 (4) 523-526
  • 90 Foki T, Vanbellingen T, Lungu C , et al. Limb-kinetic apraxia affects activities of daily living in Parkinson's disease: a multi-center study. Eur J Neurol 2016; 23 (8) 1301-1307
  • 91 Heldner MR, Vanbellingen T, Bohlhalter S, Mattle HP, Müri RM, Kamm CP. Coin rotation task: a valid test for manual dexterity in multiple sclerosis. Phys Ther 2014; 94 (11) 1644-1651
  • 92 Helmich RC, Dirkx MF. Pathophysiology and management of parkinsonian tremor. Semin Neurol 2017; 37: 000-000
  • 93 Hess CW, Pullman SL. Tremor: clinical phenomenology and assessment techniques. Tremor Other Hyperkinet Mov (N Y) 2012; 2: 2
  • 94 Hughes AJ, Daniel SE, Blankson S, Lees AJ. A clinicopathologic study of 100 cases of Parkinson's disease. Arch Neurol 1993; 50 (2) 140-148
  • 95 Zach H, Dirkx M, Bloem BR, Helmich RC. The clinical evaluation of Parkinson's tremor. J Parkinsons Dis 2015; 5 (3) 471-474
  • 96 Shulman LM, Singer C, Bean JA, Weiner WJ. Internal tremor in patients with Parkinson's disease. Mov Disord 1996; 11 (1) 3-7