Relationship between motor function and psychotic symptomatology in young–adult patients with schizophrenia

Abstract

Motor abnormalities have been indicated to be a core manifestation of schizophrenia and not just motor side-effects of antipsychotics. However, little is known about whether all of the complete motor function, including fine motor function, muscle strength, and balance is linked to psychotic symptoms. Therefore, this study was to investigate association between complete motor function and psychotic symptoms in young–adult schizophrenia patients who had no extrapyramidal motor symptoms, which were assessed using the Extrapyramidal Symptom Rating Scale. Seventy schizophrenia patients were recruited. Fine motor function, muscle strength, and balance were assessed using The McCarron Assessment of Neuromuscular Development. Psychotic symptoms were assessed using the Positive and Negative Syndrome Scale. Given gender differences in muscle power, the correlation between muscle strength and psychotic symptoms was analyzed by gender separately. Partial correlation controlling for effects of the chlorpromazine equivalent dosage of antipsychotics was conducted. Better fine motor function was correlated with less-severe negative symptoms (r = − 0.49, p < 0.001) in the total sample. In men, better muscle strength was correlated with more severe positive symptoms and less-severe negative symptoms (r = 0.41, p = 0.008; r = − 0.55, p < 0.001). The link between motor function and psychotic symptoms may support the cerebellar and basal ganglia hypotheses of schizophrenia, proposing that diverse schizophrenia symptoms may share the same neural deficiency, that is, dysfunction of cerebellum or basal ganglia. Considering the moderate-to-strong association between muscle strength and psychotic symptoms, muscle strength might be a powerful physical predictor of psychotic progression.

This is a preview of subscription content, log in to check access.

References

  1. 1.

    Mittal VA, Bernard JA, Northoff G (2017) What can different motor circuits tell us about psychosis? An RDoC perspective. Schizophr Bull 43:949–955

    PubMed  PubMed Central  Google Scholar 

  2. 2.

    Mittal VA (2016) Cross-cutting advancements usher in a new era for motor research in psychosis. Schizophr Bull 42:1322–1325

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Walther S, Strik W (2012) Motor Symptoms and Schizophrenia. Neuropsychobiology 66:77–92

    PubMed  Google Scholar 

  4. 4.

    Haddad PM, Mattay VS (2011) Neurological complications of antipsychotic drugs. In: Weinberger DR, Harrison PJ (eds) Schizophrenia. Wiley-Blackwell, West Sussex, pp 561–576

    Google Scholar 

  5. 5.

    Pappa S, Dazzan P (2009) Spontaneous movement disorders in antipsychotic-naive patients with first-episode psychoses: a systematic review. Psychol Med 39:1065–1076

    CAS  PubMed  Google Scholar 

  6. 6.

    Koning JPF, Tenback DE, van Os J, Aleman A, Kahn RS, van Harten PN (2010) Dyskinesia and parkinsonism in antipsychotic-naive patients with schizophrenia, first-degree relatives and healthy controls: a meta-analysis. Schizophr Bull 36:723–731

    PubMed  Google Scholar 

  7. 7.

    Kindler J, Schultze-Lutter F, Michel C, Martz-Irngartinger A, Linder C, Schmidt SJ et al (2016) Abnormal involuntary movements are linked to psychosis-risk in children and adolescents: results of a population-based study. Schizophr Res 174:58–64

    PubMed  Google Scholar 

  8. 8.

    Mittal VA, Neumann C, Saczawa M, Walker EF (2008) Longitudinal progression of movement abnormalities in relation to psychotic symptoms in adolescents at high risk of schizophrenia. Arch Gen Psychiatry 65:165–171

    PubMed  Google Scholar 

  9. 9.

    Callaway DA, Perkins DO, Woods SW, Liu L, Addington J (2014) Movement abnormalities predict transitioning to psychosis in individuals at clinical high risk for psychosis. Schizophr Res 159:263–266

    PubMed  PubMed Central  Google Scholar 

  10. 10.

    Mittal VA, Walker EF (2007) Movement abnormalities predict conversion to axis I psychosis among prodromal adolescents. J Abnorm Psychol 116:796–803

    PubMed  Google Scholar 

  11. 11.

    Mittal VA, Tessner KD, Trottman HD, Esterberg M, Dhruv SH, Simeonova DI et al (2007) Movement abnormalities and the progression of prodromal symptomatology in adolescents at risk for psychotic disorders. J Abnorm Psychol 116:260–267

    PubMed  Google Scholar 

  12. 12.

    Dean DJ, Kent JS, Bernard JA, Orr JM, Gupta T, Pelletier-Baldelli A et al (2015) Increased postural sway predicts negative symptom progression in youth at ultrahigh risk for psychosis. Schizophr Res 162:86–89

    PubMed  PubMed Central  Google Scholar 

  13. 13.

    Bernard JA, Dean DJ, Kent JS, Orr JM, Pelletier-Baldelli A, Lunsford-Avery JR et al (2014) Cerebellar networks in individuals at ultra high-risk of psychosis: impact on postural sway and symptom severity. Hum Brain Mapp 35:4064–4078

    PubMed  PubMed Central  Google Scholar 

  14. 14.

    Gebhardt S, Hartling F, Hanke M, Theisen FM, von Georgi R, Grant P et al (2008) Relations between movement disorders and psychopathology under predominantly atypical antipsychotic treatment in adolescent patients with schizophrenia. Eur Child Adolesc Psychiatry 17:44–53

    PubMed  Google Scholar 

  15. 15.

    Peralta V, Cuesta MJ (2011) Neuromotor abnormalities in neuroleptic-naive psychotic patients: antecedents, clinical correlates, and prediction of treatment response. Compr Psychiatry 52:139–145

    PubMed  Google Scholar 

  16. 16.

    Bilder RM, Goldman RS, Robinson D, Reiter G, Bell L, Bates JA et al (2000) Neuropsychology of first-episode schizophrenia: initial characterization and clinical correlates. Am J Psychiatry 157:549–559

    CAS  PubMed  Google Scholar 

  17. 17.

    Docx L, Morrens M, Bervoets C, Hulstijn W, Fransen E, De Hert M et al (2012) Parsing the components of the psychomotor syndrome in schizophrenia. Acta Psychiatr Scand 126:256–265

    CAS  PubMed  Google Scholar 

  18. 18.

    McCarron LT (1997) McCarron assessment of neuromuscular development (MAND): fine and gross motor abilities. McCarron-Dial Systems, Dallas

    Google Scholar 

  19. 19.

    Dazzan P, Murray RM (2002) Neurological soft signs in first-episode psychosis: a systematic review. Br J Psychiatry 181:S50–S57

    Google Scholar 

  20. 20.

    Chan RCK, Xu T, Heinrichs RW, Yu Y, Wang Y (2010) Neurological soft signs in schizophrenia: a meta-analysis. Schizophr Bull 36:1089–1104

    PubMed  Google Scholar 

  21. 21.

    Picard H, Amado I, Mouchet-Mages S, Olie JP, Krebs MO (2008) The role of the cerebellum in schizophrenia: an update of clinical, cognitive, and functional evidences. Schizophr Bull 34:155–172

    PubMed  Google Scholar 

  22. 22.

    Andreasen NC, Pierson R (2008) The role of the cerebellum in schizophrenia. Biol Psychiatry 64:81–88

    PubMed  PubMed Central  Google Scholar 

  23. 23.

    Andreasen NC, Nopoulos P, O’Leary DS, Miller DD, Wassink T, Flaum L (1999) Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biol Psychiatry 46:908–920

    CAS  PubMed  Google Scholar 

  24. 24.

    Andreasen NC, Paradiso S, O’Leary DS (1998) “Cognitive dysmetria” as an integrative theory of schizophrenia: a dysfunction in cortical-subcortical-cerebellar circuitry? Schizophr Bull 24:203–218

    CAS  PubMed  Google Scholar 

  25. 25.

    Abboud R, Noronha C, Diwadkar VA (2017) Motor system dysfunction in the schizophrenia diathesis: neural systems to neurotransmitters. Eur Psychiatry 44:125–133

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Strick PL, Dum RP, Fiez JA (2009) Cerebellum and nonmotor function. Annu Rev Neurosci 32:413–434

    CAS  PubMed  Google Scholar 

  27. 27.

    Middleton FA, Strick PL (1998) Cerebellar output: motor and cognitive channels. Trends Cogn Sci 2:348–354

    CAS  PubMed  Google Scholar 

  28. 28.

    Utter AA, Basso MA (2008) The basal ganglia: an overview of circuits and function. Neurosci Biobehav Rev 32:333–342

    PubMed  Google Scholar 

  29. 29.

    Manto M, Bower JM, Conforto AB, Delgado-Garcia JM, da Guarda SNF, Gerwig M et al (2012) Consensus paper: roles of the cerebellum in motor control—the diversity of ideas on cerebellar involvement in movement. Cerebellum 11:457–487

    PubMed  PubMed Central  Google Scholar 

  30. 30.

    Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31:236–250

    CAS  PubMed  Google Scholar 

  31. 31.

    American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders. Author, Washington, DC

    Google Scholar 

  32. 32.

    Chouinard G, Ross-Chouinard A, Annable L, Jones B (1980) The extrapyramidal symptom rating scale. Can J Neurol Sci 7:233–239

    Google Scholar 

  33. 33.

    Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13:261–276

    CAS  Google Scholar 

  34. 34.

    Cheng JJ, Ho H, Chang CJ, Lan SY, Hwu HG (1996) Positive and negative syndrome scale (PANSS): establishment and reliability study of a Mandarin Chinese language version. Chin Psychiatry 10:251–258

    Google Scholar 

  35. 35.

    Leucht S, Samara M, Heres S, Patel MX, Woods SW, Davis JM (2014) Dose equivalents for second-generation antipsychotics: the minimum effective dose method. Schizophr Bull 40:314–326

    PubMed  PubMed Central  Google Scholar 

  36. 36.

    American Psychiatric Association (2006) Practice guidelines for the treatment of psychiatric disorders: compendium. Author, Arlington

    Google Scholar 

  37. 37.

    Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

    Google Scholar 

  38. 38.

    Ehrsson HH, Fagergren A, Jonsson T, Westling G, Johansson RS, Forssberg H (2000) Cortical activity in precision- versus power-grip tasks: an fMRI study. J Neurophysiol 83:528–536

    CAS  PubMed  Google Scholar 

  39. 39.

    Dettmers C, Fink GR, Lemon RN, Stephan KM, Passingham RE, Silbersweig D et al (1995) Relation between cerebral activity and force in the motor areas of the human brain. J Neurophysiol 74:802–815

    CAS  PubMed  Google Scholar 

  40. 40.

    Cramer SC, Weisskoff RM, Schaechter JD, Nelles G, Foley M, Finklestein SP et al (2002) Motor cortex activation is related to force of squeezing. Hum Brain Mapp 16:197–205

    PubMed  Google Scholar 

  41. 41.

    Mehler-Wex C, Riederer P, Gerlach M (2006) Dopaminergic dysbalance in distinct basal ganglia neurocircuits: implications for the pathophysiology of Parkinson’s disease, schizophrenia and attention deficit hyperactivity disorder. Neurotox Res 10:167–179

    CAS  PubMed  Google Scholar 

  42. 42.

    Walker EF (1994) Developmentally moderated expressions of the neuropathology underlying schizophrenia. Schizophr Bull 20:453–480

    CAS  PubMed  Google Scholar 

  43. 43.

    Bernard JA, Orr JM, Mittal VA (2017) Cerebello-thalamo-cortical networks predict positive symptom progression in individuals at ultra-high risk for psychosis. Neuroimage Clin 14:622–628

    PubMed  PubMed Central  Google Scholar 

  44. 44.

    Walther S, Stegmayer K, Federspiel A, Bohlhalter S, Wiest R, Viher PV (2017) Aberrant hyperconnectivity in the motor system at rest is linked to motor abnormalities in schizophrenia spectrum disorders. Schizophr Bull 43:982–992

    PubMed  PubMed Central  Google Scholar 

  45. 45.

    Hoppenbrouwers SS, Schutter D, Fitzgerald PB, Chen R, Daskalakis ZJ (2008) The role of the cerebellum in the pathophysiology and treatment of neuropsychiatric disorders: a review. Brain Res Rev 59:185–200

    CAS  PubMed  Google Scholar 

  46. 46.

    Torrey EF (2002) Studies of individuals with schizophrenia never treated with antipsychotic medications: a review. Schizophr Res 58:101–115

    PubMed  Google Scholar 

  47. 47.

    Shenton ME, Dickey CC, Frumin M, McCarley RW (2001) A review of MRI findings in schizophrenia. Schizophr Res 49:1–52

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Bernard JA, Mittal VA (2014) Cerebellar-motor dysfunction in schizophrenia and psychosis-risk: the importance of regional cerebellar analysis approaches. Front Psychiatry 5:1–14

    Google Scholar 

  49. 49.

    Mittal VA, Orr JM, Turner JA, Pelletier AL, Dean DJ, Lunsford-Avery J et al (2013) Striatal abnormalities and spontaneous dyskinesias in non-clinical psychosis. Schizophr Res 151:141–147

    PubMed  Google Scholar 

  50. 50.

    Vancampfort D, Probst M, Scheewe T, De Herdt A, Sweers K, Knapen J et al (2013) Relationships between physical fitness, physical activity, smoking and metabolic and mental health parameters in people with schizophrenia. Psychiatry Res 207:25–32

    PubMed  Google Scholar 

  51. 51.

    Mamah D, Wang L, Barch D, de Erausquin GA, Gado M, Csernansky JG (2007) Structural analysis of the basal ganglia in schizophrenia. Schizophr Res 89:59–71

    PubMed  Google Scholar 

  52. 52.

    Martinelli C, Rigoli F, Shergill SS (2017) Aberrant force processing in schizophrenia. Schizophr Bull 43:417–424

    PubMed  Google Scholar 

  53. 53.

    Delevoye-Turrell Y, Giersch A, Danion JM (2003) Abnormal sequencing of motor actions in patients with schizophrenia: evidence from grip force adjustments during object manipulation. Am J Psychiatry 160:134–141

    PubMed  Google Scholar 

  54. 54.

    Heckers S (2000) Neural models of schizophrenia. Dialogues Clin Neurosci 2:267–279

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Fuller R, Jahanshahi M (1999) Concurrent performance of motor tasks and processing capacity in patients with schizophrenia. J Neurol Neurosurg Psychiatry 66:668–671

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Bervoets C, Docx L, Sabbe B, Vermeylen S, Van Den Bossche MJ, Morsel A et al (2014) The nature of the relationship of psychomotor slowing with negative symptomatology in schizophrenia. Cogn Neuropsychiatry 19:36–46

    PubMed  Google Scholar 

  57. 57.

    Morrens M, Hulstijn W, Sabbe B (2007) Psychomotor slowing in schizophrenia. Schizophr Bull 33:1038–1053

    PubMed  Google Scholar 

  58. 58.

    Kuhn S, Romanowski A, Schilling C, Banaschewski T, Barbot A, Barker GJ et al (2012) Manual dexterity correlating with right lobule VI volume in right-handed 14-year-olds. Neuroimage 59:1615–1621

    PubMed  Google Scholar 

  59. 59.

    Koop MM, Shivitz N, Bronte-Stewart H (2008) Quantitative measures of fine motor, limb, and postural bradykinesia in very early stage, untreated Parkinson’s disease. Mov Disord 23:1262–1268

    PubMed  Google Scholar 

  60. 60.

    Galeno R, Molina M, Guirao M, Isoardi R (2004) Severity of negative symptoms in schizophrenia correlated to hyperactivity of the left globus pallidus and the right claustrum. A PET study. World J Biol Psychiatry 5:20–25

    PubMed  Google Scholar 

  61. 61.

    Horak FB, Dimitrova D, Nutt JG (2005) Direction-specific postural instability in subjects with Parkinson’s disease. Exp Neurol 193:504–521

    PubMed  Google Scholar 

  62. 62.

    Jacobs BL, Fornal CA (1997) Serotonin and motor activity. Curr Opin Neurobiol 7:820–825

    CAS  PubMed  Google Scholar 

  63. 63.

    Rijcken CAW, Monster TBM, Brouwers J, de Jong-van den Berg LTW (2003) Chlorpromazine equivalents versus defined daily doses: how to compare antipsychotic drug doses? J Clin Psychopharmacol 23:657–659

    CAS  PubMed  Google Scholar 

  64. 64.

    Simpson EH, Kellendonk C, Kandel E (2010) A possible role for the striatum in the pathogenesis of the cognitive symptoms of schizophrenia. Neuron 65:585–596

    CAS  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Koshiyama D, Fukunaga M, Okada N, Yamashita F, Yamamori H, Yasuda Y et al (2018) Role of subcortical structures on cognitive and social function in schizophrenia. Sci Rep 8:9

    Google Scholar 

  66. 66.

    Cuesta MJ, Garcia de Jalon E, Campos MS, Moreno-Izco L, Lorente-Omenaca R, Sanchez-Torres AM et al (2018) Motor abnormalities in first-episode psychosis patients and long-term psychosocial functioning. Schizophr Res 200:97–103

    PubMed  Google Scholar 

  67. 67.

    Chuang LL, Wu CY, Lin KC (2012) Reliability, validity, and responsiveness of myotonometric measurement of muscle tone, elasticity, and stiffness in patients with stroke. Arch Phys Med Rehabil 93:532–540

    PubMed  Google Scholar 

  68. 68.

    Lam WK, Mok D, Lee WC, Chen B (2015) Reliability and asymmetry profiles of myotonometric measurements in healthy skeletal muscles. J Nov Physiother 5:245

    Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Yu-Lin Liu, Mr. Shyh-Hung Li, and Ms. Chi-Yueh Hsu for the support of subject recruitment and data collection.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Li-Chieh Kuo.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wang, S., Ouyang, W., Wu, M. et al. Relationship between motor function and psychotic symptomatology in young–adult patients with schizophrenia. Eur Arch Psychiatry Clin Neurosci 270, 373–382 (2020). https://doi.org/10.1007/s00406-019-01004-1

Download citation

Keywords

  • Psychosis
  • Cerebellum
  • Basal ganglia
  • Muscle strength
  • Fine motor