Journal of Neural Transmission

, Volume 121, Issue 4, pp 443–450 | Cite as

Gait control and executive dysfunction in early schizophrenia

  • Elise Lallart
  • Roland Jouvent
  • François R. Herrmann
  • Fernando Perez-Diaz
  • Xavier Lallart
  • Olivier Beauchet
  • Gilles Allali
Psychiatry and Preclinical Psychiatric Studies - Original Article

Abstract

Dysexecutive functioning, which is described as an enduring core feature of schizophrenia, has been associated with gait disorders. However, few studies have reported gait disorders in schizophrenia patients. The objective of this study was to examine the association between executive dysfunction and gait performance in recent-onset schizophrenia patients using the dual task paradigm. Thirty-two subjects participated to the study: 17 with recent-onset schizophrenia and 15 healthy age-matched controls. Executive functions were evaluated using the Frontal Assessment Battery, Stroop and Trail-Making tests. Mean values and coefficients of variation (CV) of the temporal gait parameters while single tasking (just walking) and while dual tasking (walking and forward counting, walking and backward counting, walking and verbal fluency) were measured using the SMTEC®-footswitch system. We focused on the CV of stride time as this measure has been shown to be the most representative parameter of higher gait control. A strong effect of the stride time was found in the group factor for the verbal fluency dual-task when compared to controls (Cohen’s d mean = 1.28 and CV = 1.05). The effect was lower in the other dual tasks, and insignificant in the single task of walking. This study shows that patients exhibit higher stride-to-stride variability while dual tasking than controls. It also shows a stronger impact of verbal fluency on gait regularity compared to the other dual tasks revealing a relationship between the executive dysfunction and gait modification. Those results are in line with the idea that schizophrenia implies not only cognitive but also motor functioning and coordination impairment.

Keywords

Gait control Schizophrenia Executive function Dual task 

References

  1. Allali G, Kressig RW, Assal E, Herrmann FR, Beauchet O (2005) A Dual-task related stride time variability among demented older adults with dysexecutive functions. Gait Posture 21(1):S51CrossRefGoogle Scholar
  2. Allali G, Kressig R, Assal F, Herrmann F, Dubost V, Beauchet O (2007) Changes in gait while backward counting in demented older adults with frontal lobe dysfunction. Gait Posture 26:572–576PubMedCrossRefGoogle Scholar
  3. Allali G, Dubois B, Assal F, Lallart E, de Souza LC, Bertoux M, Annweiler C, Herrmann FR, Levy R, Beauchet O (2010) Frontotemporal dementia: pathology of gait? Mov Disord 25(6):723–729CrossRefGoogle Scholar
  4. Amboni M, Cozzolino A, Longo K, Picillo M, Barone P (2008) Freezing of gait and executive functions in patients with Parkinson’s disease. Mov Disord 23(3):395–400PubMedCrossRefGoogle Scholar
  5. Bakker M, De Lange FP, Helmich RC, Scheeringa R, Bloem BR, Toni I (2008) Cerebral correlates of motor imagery of normal and precision gait. Neuroimage 41:998–1010PubMedCrossRefGoogle Scholar
  6. Beauchet O, Allali G, Berrut G, Hommet C, Dubost V, Assal F (2008a) Gait analysis in demented subjects: interest and perspectives. Neuropsychiatr Dis Treat 4:155–160PubMedCentralPubMedCrossRefGoogle Scholar
  7. Beauchet O, Herrmann F, Grandjean R, Dubost V, Allali G (2008b) Concurrent validity of SMTEC footswitches system for the measurement of temporal gait parameters. Gait Posture 27:156–159PubMedCrossRefGoogle Scholar
  8. Bersani G, Quartini A, Paolemili M, Clemente R, Iannitelli A, Di Biasi C, Gualdi G (2011) Neurological soft signs and corpus callosum morphology in schizophrenia. Neurosci Lett 499:170–174PubMedCrossRefGoogle Scholar
  9. Birn RM, Kenworthly L, Case L, Caravella R, Jones TB, Bandettini PA, Martin A (2010) Neural systems supporting lexical search gided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency. Neuroimage 49:1099–1107PubMedCentralPubMedCrossRefGoogle Scholar
  10. Bleuler E (1911) Dementia praecox or the group of schizophrenias. International Press Universities, New YorkGoogle Scholar
  11. Bozikas V, Kosmidis M, Karavatos A (2005) Disproportionate impairment in semantic verbal fluency in schizophrenia: differential deficit in clustering. Schizophr Res 74(205):51–59PubMedCrossRefGoogle Scholar
  12. Chan R, Chen E, Law C (2006) Specific executive dysfunction in patients with first-episode medication-naïve schizophrenia. Schizophr Res 82(1):51–64PubMedCrossRefGoogle Scholar
  13. Chan RC, Xu TR, Heinrichs W, Yue WY, Wang Y (2009) Neurological Soft Signs in Schizophrenia: a meta-analysis. Schizophr Bull 36(6):1089–1104PubMedCentralPubMedCrossRefGoogle Scholar
  14. Collie A, Darekar A, Maruff P, Snyder P, Huggins JP (2006) Cognitive testing in early-phase clinical trials: development of a rapid computerized test battery and application in a simulated Phase I study. Eur Neuropsychopharmacol 16(4):S274–S275CrossRefGoogle Scholar
  15. Delval A, Krystkowiak P, Delliaux M, Blatt JL, Derambure P, Destée A, Defebvre L (2008) Effect of external cueing on gait in Huntington’s disease. Mov Disord 23(10):1446–1452PubMedCrossRefGoogle Scholar
  16. Dubois B, Slachevsky A, Litvan I, Pillon B (2000) The FAB: a frontal assessment battery at bedside. Neurology 55:1621–1626PubMedCrossRefGoogle Scholar
  17. Elvevag B, Weinstock D, Akil M, Kleinman JE, Goldberg T (2001) A comparison of verbal tasks in schizophrenic patients and normal controls. Schizophr Res 51:119–126PubMedCrossRefGoogle Scholar
  18. First MB, Spitzer RL, Gibbon M, Williams JBW (1996) Structured clinical interview for the DSM-IV axis I disorders, Clinical version (SCID-CV). American Psychiatric Press, Washington, DCGoogle Scholar
  19. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198PubMedCrossRefGoogle Scholar
  20. Gazzaley A, D’Esposito M (2006) Neural networks: an empirical neuroscience approach toward understanding cognition. Cortex 42:1037–1040CrossRefGoogle Scholar
  21. Gupta S, Andreasen N, Arndt S, Flaum M, Schults S, Hubbard W, Smith M (1995) Neurological soft signs in neuroleptic-naïve and neuroleptic-treated schizophrenic patients and in normal comparaison subjects. Am J Psychiatry 152:191–196PubMedGoogle Scholar
  22. Harada T, Miyai I, Suzuki M, Kubota K (2009) Gait capacity affects cortical activation patterns related to Speedy control in the elderly. Exp Brain Res 193:445–454PubMedCrossRefGoogle Scholar
  23. Harvey PD, Bowe CR, Loebel A, Warrington L (2004) Cognitive improvement andneuropsychological normalization with ziprasidone or olanzapine: results of a 6-month study. Eur Neuropsychopharmacol 14(3):S294CrossRefGoogle Scholar
  24. Hausdorff J, Yogev G, Springer S, Simon E, Giladi N (2005) Walking is more like catching than tapping: gait in the elderly as complex cognitive task. Exp Brain Res 164:541–548PubMedCrossRefGoogle Scholar
  25. Hirjak D, Wolf R, Stieltjes B, Hauser T, Seidl U, Thiermann U, Schröder J, Thomann P (2013) Neurological soft signs and brainstem morphology in frist-episode schizophrenia. Neuropsychobiology 68(2):91–99PubMedCrossRefGoogle Scholar
  26. Iseki K, Hanakawa T, Shinozaki J, Nankaku M, Fukuyama H (2008) Neural mechanisms involved in mental imagery and observation of gait. Neuroimage 41:1021–1031PubMedCrossRefGoogle Scholar
  27. Kasparek T, Rehulova J, Kerkovsky M, Sprlakova A, Mechl M, Mikl M (2012) Cortico-cerebellar functional connectivity and sequencing of movements in schizophrenia. BMC Psychiatry 12:12–17CrossRefGoogle Scholar
  28. Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13:261–276PubMedCrossRefGoogle Scholar
  29. Lallart E, Jouvent R, Herrmann F, Beauchet O, Allali G (2012) Gait and motor imagery of gate in early schizophrenia. Psychiatry Res 198(3):366–370PubMedCrossRefGoogle Scholar
  30. Lecrubier Y, Sheehan D, Weiller E (1997) The Mini International Neuropsychiatric Interview (M.I.N.I): a short diagnostic structured interview: reliability and validity according to the CIDI. Eur Psychiatry 12:224–231CrossRefGoogle Scholar
  31. Lemke M, Wendorff T, Mieth B, Buhl K, Linnemann M (2000) Spatiotemporal gait patterns during over ground locomotion in major depression compared with healthy controls. J Psychiatr Res 34(4–5):277–283PubMedCrossRefGoogle Scholar
  32. Lepow L, Van Sweringen J, Strutt AM, Jawaid A, Macadam C, Harati Y, Schulz PE, York MK (2010) Frontal and temporal lobe involvement on verbal fluency measures in amyotrophic lateral sclerosis. Clin Exp Neuropsychol. 13:1–10Google Scholar
  33. Putzhammer A, Heindl B, Broll K, Pfeiff L, Perfahl M, Hajak G (2004) Spatial and temporal parameters of gait disturbances in schizophrenic patients. Schizophr Res 69(2–3):159–166PubMedCrossRefGoogle Scholar
  34. Royer A, Christian F, Schneider G, Grosselin A, Pellet J, Barral F, Laurent B, Brouillet D, Lang F (2009) Brain activation during executive process in schizophrenia. Psychiatry Res: Neuroimaging 173(3):170–176PubMedCrossRefGoogle Scholar
  35. Ruff RM, Light RH, Parker SB, Levin HS (1997) The psychological construct of word fluency. Brain Lang 57:394–405PubMedCrossRefGoogle Scholar
  36. Saykin AJ, Shtasel DL, Gur RE, Kester DB, Mozley LH, Stafiniak P, Gur RC (1994) Neurpsychological deficits in neuroleptic naïve patients with first episode schizophrenia. Arch Gen Psychiatry 51(2):124–131PubMedCrossRefGoogle Scholar
  37. Shallice T, Burgess P, Schon F, Baxter D (1989) The origins of utilization behavior. Brain 112:1587–1598PubMedCrossRefGoogle Scholar
  38. Sheridan PL, Solomont J, Kowall N, Hausdorff JM (2003) Influence of executive function on locomotor function: divided attention increases gait variability in Alzheimer’s disease. J Am Geriatr Soc 51:1633–1637PubMedCrossRefGoogle Scholar
  39. Strauss E, Sherman E, Spreem O (2006) A compendium of neuropsychological tests: administration, norms and commentary, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  40. Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643–662CrossRefGoogle Scholar
  41. Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, Kubota K (2004) Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage 23:1020–1026PubMedCrossRefGoogle Scholar
  42. Townsend LA, Malla AK, Norman MG (2001) Cognitive functioning in stabilized first-episode psychosis patients. Psychiatry Res 104:119–131PubMedCrossRefGoogle Scholar
  43. U.S. War Department AGsO (1944) The new army individual test of general mental ability. Psych Bull 41:532–538CrossRefGoogle Scholar
  44. Van Beilen M, Pijnenborg M, van Zomeren E, van den Bosch R, Withaar F, Boumac A (2004) What is measured by verbal fluency tests in schizophrenia? Schizophr Res 69(2–3):267–276PubMedCrossRefGoogle Scholar
  45. Van der Meulen M, Allali G, Rieger S, Assal F, Vuilleumier P (2012) The influence of individual motor imagery ability on cerebral recruitment during gait imagery. Hum Brain Mapp. doi:10.1002/hbm.22192 PubMedGoogle Scholar
  46. Wang J, Wai Y, Weng Y, Ng K, Huang Y, Ying L, Liu H, Wang C (2009) Functional MRI in the assessment of cortical activation during gait-related imaginary tasks. J Neural Transm 116:1087–1092PubMedCrossRefGoogle Scholar
  47. Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM (2005) Dual tasking, gait rhythmicity, and Parkinson’s disease: which aspects of gait are attention demanding? Eur J Neurosci 22(5):1248–1256PubMedCrossRefGoogle Scholar
  48. Zhao Q, Li Z, Huang J, Yan C, Dazzan P, Pantelis C, Cheung E, Lui S, Chan R (2013) Neurological soft signs are not “soft” in brain structure and functional networks: evidence from ALE meta-analysis. Schizophrenia BulletinGoogle Scholar

Copyright information

© European Union 2013

Authors and Affiliations

  • Elise Lallart
    • 1
  • Roland Jouvent
    • 1
  • François R. Herrmann
    • 2
  • Fernando Perez-Diaz
    • 1
  • Xavier Lallart
    • 3
  • Olivier Beauchet
    • 4
    • 5
  • Gilles Allali
    • 6
  1. 1.Emotion Center, CNRS UMR 3246Hôpital de la Pitié-SalpêtrièreParisFrance
  2. 2.Department of Rehabilitation and Geriatrics, Geneva University HospitalsUniversity of GenevaGenevaSwitzerland
  3. 3.Ville-Evrard Psychiatric HospitalNeuilly-sur-seineFrance
  4. 4.Department of Neuroscience, Geriatrics DivisionAngers University HospitalAngersFrance
  5. 5.University of Angers, UNAMAngersFrance
  6. 6.Department of Neurology and Faculty of MedicineGeneva University HospitalsGenevaSwitzerland

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