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Predictive eye and hand movements are differentially affected by schizophrenia

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Abstract

Background

Schizophrenic patients are known to have problems suppressing reflexive eye movements. This is considered to indicate a dysfunction in prefrontal cortex. As the eye and hand motor systems are tightly coupled, we investigated whether predictive hand movements and eye-hand coordination are unimpaired in schizophrenic patients.

Method

Saccades and hand movements of 19 patients during an acute schizophrenic episode and 19 controls were measured in a task in which the predictability of target timing was varied.

Results

Schizophrenic patients generated more anticipatory and less visually triggered saccades than controls with both non-predictable and predictable target timing. Anticipatory saccades in the wrong direction were clearly directed towards previous target positions, indicating that they are indicators of erroneous prediction rather than of fixation instability. In contrast to saccades, the number of anticipatory and visually triggered hand movements was the same in patients as in controls. As a consequence, patients took longer to initiate a hand movement after a saccade than controls.

Conclusion

Schizophrenic patients show increased predictive saccadic activity, but no qualitative changes in predictive saccades. Since prediction itself was not disturbed, the patients’ deficit rather lies in the suppression or gating of anticipatory saccades than in their generation. This may be explained by a selective dysfunction of the basal ganglia oculomotor loop. As predictive hand movements were unimpaired, the problems in eye-hand coordination as expressed by a longer initiation time of hand movements relative to saccades are a direct consequence of impaired predictive saccadic behaviour.

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References

  1. Abrams RA, Meyer DE, Kornblum S (1990) Eye-hand coordination: oculomotor control in rapid aimed limb movements. J Exp Psychol: Hum Percept Perform 16:248–267

    Article  CAS  Google Scholar 

  2. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci 9:357–381

    Article  CAS  PubMed  Google Scholar 

  3. Becker W (1989) Metrics. In: Wurtz RH, Goldberg ME (eds.) The Neurobiology of Saccadic Eye Movements, Elsevier, Amsterdam (Vol. 3), pp. 13–61

  4. Bekkering H, Adam JJ, van den Aarssen A, Kingma H, Whiting HT (1995) Interference between saccadic eye and goal-directed hand movements. Exp Brain Res 106:475–484

    Article  CAS  PubMed  Google Scholar 

  5. Bender S, Dittmann-Balcar A, Schall U, Wolstein J, Klimke A, Riedel M, Vorbach EU, Kuhn KU, Lambert M, Dittmann RW, Naber D (2006) Influence of atypical neuroleptics on executive functioning in patients with schizophrenia: a randomized, double-blind comparison of olanzapine vs. clozapine. Int J Neuropsychopharmacol 9:135–145

    Article  CAS  PubMed  Google Scholar 

  6. Biguer B, Jeannerod M, Prablanc C (1982) The coordination of eye, head, and arm movements during reaching at a single visual target. Exp Brain Res 46:301–304

    Article  CAS  PubMed  Google Scholar 

  7. Brown JW, Bullock D, Grossberg S (2004) How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades. Neural Netw 17:471–510

    Article  PubMed  Google Scholar 

  8. Busatto GF, Kerwin RW (1997) Schizophrenia, psychosis, and the basal ganglia Psychiatric Clin N Am 20:897–910

    Article  CAS  Google Scholar 

  9. Carpenter RHS, Williams MLL (1995) Neural computation of log likelihood in control of saccadic eye movements. Nature 377:59–62

    Article  CAS  PubMed  Google Scholar 

  10. Clementz BA, McDowell JE, Zisook S (1994) Saccadic system functioning among schizophrenia patients and their first-degree biological relatives. J Abnorm Psychol 103:277–287

    Article  CAS  PubMed  Google Scholar 

  11. Crawford TJ, Haeger B, Kennard C, Reveley MA, Henderson L (1995a) Saccadic abnormalities in psychotic patients. I. Neuroleptic-free psychotic patients. Psychol Med 25:461–471

    Google Scholar 

  12. Crawford TJ, Haeger B, Kennard C, Reveley MA, Henderson L (1995b) Saccadic abnormalities in psychotic patients. II. The role of neuroleptic treatment. Psychol Med 25:473–483

    Google Scholar 

  13. Di Lollo V (1980) Temporal integration in visual memory. Exp Psychol Gen 109:75–97

    Article  Google Scholar 

  14. Dreher JC, Trapp W, Banquet JP, Keil M, Gunther W, Burnod Y (1999) Planning dysfunction in schizophrenia: impairment of potentials preceding fixed/free and single/sequence of self-initiated finger movements. Exp Brain Res 124:200–214

    Article  CAS  PubMed  Google Scholar 

  15. Fischer B, Weber H (1993) Modes of saccade generation and their attentional control. Behav Brain Sci 16:595–610

    Article  Google Scholar 

  16. Fischer B, Weber H, Biscaldi M, Aiple F, Otto P, Stuhr V (1993) Separate populations of visually guided saccades in humans: reaction times and amplitudes. Exp Brain Res 92:528–541

    Article  CAS  PubMed  Google Scholar 

  17. Fox PT, Fox JM, Raichle ME, Burde RM (1985) The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomography study. J Neurophysiol 54:348–369

    CAS  PubMed  Google Scholar 

  18. Frens MA, Erkelens CJ (1991) Coordination of hand movements and saccades: evidence for a common and a separate pathway. Exp Brain Res 85:682–690

    Article  CAS  PubMed  Google Scholar 

  19. Fukushima J, Fukushima K, Chiba T, Tanaka S, Yamashita I, Kato M (1988) Disturbances of voluntary control of saccadic eye movements in schizophrenic patients. Biol Psychiat 23:670–677

    Article  CAS  PubMed  Google Scholar 

  20. Fukushima J, Fukushima M, Morita N, Yamashita I (1990a) Further analysis of the control of voluntary sacadic eye movements in schizophrenic patients. Biol Psychiat 28:943–958

    Google Scholar 

  21. Fukushima J, Morita N, Fukushima K, Chiba T, Tanaka S, Yamashita I (1990b) Voluntary control of saccadic eye movements in patients with schizophrenic and affective disorders. J Psychiat Res 24:9–24

    Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Gagnon D, O’Driscoll GA, Petrides M, Pike GB (2000) The effect of spatial and temporal information on saccades and neural activity in oculomotor structures. Brain 125:123–139

    Article  Google Scholar 

  24. Gangadhar BN, Jayakumar PN, Subbakrishna DK, Janakiramaiah N, Keshavan MS (2004) Basal ganglia high-energy phosphate metabolism in neuroleptic-naive patients with schizophrenia: a 31-phosphorus magnetic resonance spectroscopic study. Am J Psychiat 161:1304–1306

    Article  CAS  PubMed  Google Scholar 

  25. Granholm E (1992) Processing resource limitations in schizophrenia: implications for predicting medication response and planning attentional training. In: Margolin DI (ed) Cognitive neuropsychology in clinical practice. Oxford University Press, New York, pp 43–69

    Google Scholar 

  26. Granholm E, Asarnow RF, Marder SR (1996) Dual-task performance operating characteristics, resource limitations, and automatic processing in schizophrenia. Neuropsychology 10:11–21

    Article  Google Scholar 

  27. Guitton D, Buchtel HA, Douglas RM (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Exp Brain Res 58:455–472

    Article  CAS  PubMed  Google Scholar 

  28. Guy W, Bonato RR (1970) CGI: Clinical Global Impressions. In: Manual for the ECDEU Assessment Battery. National Institute of Mental Health 12-1–12-6

  29. Hasegawa RP, Blitz AM, Geller NL, Goldberg ME (2000) Neurons in monkey prefrontal cortex that track past or predict future performance. Science 290(5497):1786–1789

    Article  CAS  PubMed  Google Scholar 

  30. Hikosaka O (1989) Role of basal ganglia in saccades. Rev Neurol (Paris) 145:580–586

    CAS  Google Scholar 

  31. Hikosaka O, Takikawa Y, Kawagoe R (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953–978

    CAS  PubMed  Google Scholar 

  32. Hommer DW, Clem T, Litman R, Pickar D (1991) Maladaptive anticipatory saccades in schizophrenia. Biol Psychiat 30:779–794

    Article  CAS  PubMed  Google Scholar 

  33. Hutton SB, Cuthbert I, Crawford TJ, Kennard C, Barnes TR, Joyce EM (2001) Saccadic hypometria in drug-naive and drug-treated schizophrenic patients: a working memory deficit? Psychophysiology 38:125–132

    CAS  PubMed  Google Scholar 

  34. Iacono WG, Tuason VB, Johnson RA (1981) Dissociation of smooth-pursuit and saccadic eye tracking in remitted schizophrencies. An ocular reaction time task that schizophrenic perform well. Arch Gen Psychiat 35:991–996

    Google Scholar 

  35. Karoumi B, Ventre-Dominey J, Dalery J (1998) Predictive saccade behavior is enhanced in schizophrenia. Cognition 68:B81–B91

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  37. Keefe RS, Seidman LJ, Christensen BK, Hamer RM, Sharma T, Sitskoorn MM, Lewine RR, Yurgelun-Todd DA, Gur RC, Tohen M, Tollefson GD, Sanger TM, Lieberman JA (2004) Comparative effect of atypical and conventional antipsychotic drugs on neurocognition in first-episode psychosis: a randomized, double-blind trial of olanzapine versus low doses of haloperidol. Am J Psychiatry 161:985–995

    Article  PubMed  Google Scholar 

  38. Kingstone A, Klein RM (1993) Visual offsets facilitate saccadic latency: does predisengagement of visuospatial attention mediate this gap effect? J Exp Psychol: Hum Percept Perform 19:1251–1265

    Article  CAS  Google Scholar 

  39. Krebs MO, Gut-Fayand A, Amado I, Daban C, Bourdel MC, Poirier MF, Berthoz A (2001) Impairment of predictive saccades in schizophrenia. Neuroreport 12:465–469

    Article  CAS  PubMed  Google Scholar 

  40. Lazzari S, Vercher JL, Buizza A (1987) Manuo-ocular coordination in target tracking. I. A model simulating human performance. Biol Cybern 77:257–266

    Article  Google Scholar 

  41. McDowell JE, Clementz BA, Wixted JT (1996) Timing and amplitude of saccades during predictive saccadic tracking in schizophrenia. Psychophysiology 33:93–101

    Article  CAS  PubMed  Google Scholar 

  42. Meisenzahl EM, Dresel S, Frodl T, Schmitt GJ, Preuss UW, Rossmuller B, Tatsch K, Mager T, Hahn K, Möller HJ (2000) D2 receptor occupancy under recommended and high doses of olanzapine: an iodine-123-iodobenzamide SPECT study. J Psychopharmacol 14:364–370

    Article  CAS  PubMed  Google Scholar 

  43. Menon V, Anagnoson AB, Glover GH, Pfefferbaum A (2001) Functional magnetic resonance imaging evidence for disrupted basal ganglia function in schizophrenia. Am J Psychiat 158:646–649

    Article  CAS  PubMed  Google Scholar 

  44. Middleton FA, Strick PL (2001) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31:236–250

    Article  Google Scholar 

  45. Milea D, Lobel E, Lehericy S, Duffau H, Rivaud-Pechoux S, Berthoz A, Pierrot-Deseilligny C (2002) Intraoperative frontal eye field stimulation elicits ocular deviation and saccade suppression. Neuroreport 13:1359–1364

    Article  PubMed  Google Scholar 

  46. Moriarty PJ, Harvey PD, Mitropoulou V, Granholm E, Silverman JM, Siever LJ (2003) Reduced processing resource availability in schizotypal personality disorder: evidence from a dual-task CPT study. J Clin Exp Neuropsych 25:335–347

    Article  Google Scholar 

  47. Möller HJ, Boyer P, Fleurot O, Rein W, PROD-ASLP Study Group (1997) Improvement of acute exacerbations of schizophrenia with amisulpride: a comparison with haloperidol. Psychopharmacology (Berl) 132:396–401

    Article  Google Scholar 

  48. Müller N, Riedel M, Scheppach C, Brandstatter B, Sokullu S, Krampe K, Ulmschneider M, Engel RR, Möller HJ, Schwarz MJ (2002) Beneficial antipsychotic effects of celecoxib add-on therapy compared to risperidone alone in schizophrenia. Am J Psychiatry 159:1029–1034

    Article  PubMed  Google Scholar 

  49. Müller N, Riedel M, Eggert T, Straube A (1999) Internally and externally guided voluntary saccades in unmedicated and medicated schizophrenic patients. Part II. Saccadic latency, gain, and fixation suppression errors. Eur Arch Psy Clin N 249:7–14

    Article  Google Scholar 

  50. Nelder JA, Wedderburn RWM (1972) Generalized linear models. J R Stat Soc A 135:370–384

    Article  Google Scholar 

  51. Nuechterlein KH (1977) Reaction time and attention in schizophrenia: a critical evaluation of the data and theories. Schiz Bull 3:373–428

    CAS  Google Scholar 

  52. Nuechterlein KH, Dawson ME (1984) Information processing and attentional functioning in the course of schizophrenic disorder. Schiz Bull 10:160–203

    CAS  Google Scholar 

  53. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  54. Paillard J (1982) The contribution of peripheral and central vision to visually guided reaching. In: Ingle DJ, Goodale MA, Mansfield RJ (eds) Analysis of visual behavior. MIT Press, Cambridge Mass, pp 367–385

    Google Scholar 

  55. Prablanc C, Echallier JF, Komilis E, Jeannerod M (1979) Optimal response of eye and hand motor systems in pointing at a visual target. I. Spatio–temporal characteristics of eye and hand movements and their relationships when varying the amount of visual information. Biol Cybern 35:113–124

    Article  CAS  PubMed  Google Scholar 

  56. Raemaekers M, Jansma JM, Cahn W, Van der Geest JN, van der Linden JA, Kahn RS, Ramsey NF (2002) Neuronal substrate of the saccadic inhibition deficit in schizophrenia investigated with 3-dimensional event-related functional magnetic resonance imaging. Arch Gen Psychiat 59:313–320

    Article  PubMed  Google Scholar 

  57. Riedel M, Müller N, Strassnig M, Spellmann I, Engel RR, Musil R, Dehning S, Douhet A, Schwarz MJ, Möller HJ (2005) Quetiapine has equivalent efficacy and superior tolerability to risperidone in the treatment of schizophrenia with predominantly negative symptoms. Eur Arch Psychiatry Clin Neurosci 255:432–437

    Article  PubMed  Google Scholar 

  58. Sailer U, Eggert T, Ditterich J, Straube A (2000) Spatial and temporal aspects of eye-hand coordination across different tasks. Exp Brain Res 134:163–173

    Article  CAS  PubMed  Google Scholar 

  59. Sailer U, Eggert T, Ditterich J, Straube A (2002a) Global effect of a nearby distractor on targeting eye and hand movements. J Exp Psychol: Hum Percept Perform 28:1432–1446

    Article  Google Scholar 

  60. Sailer U, Eggert T, Straube A (2002b) Implications of distracter effects for the organization of eye movements, hand movements, and perception. Prog Brain Res 140:341–349

    Article  Google Scholar 

  61. Sailer U, Eggert T, Straube A (2005) Impaired temporal prediction and eye-hand coordination in patients with cerebellar lesions. Behav Brain Res 160:72–87

    Article  PubMed  Google Scholar 

  62. Scarchilli K, Vercher JL (1999) The oculomanual coordination control center takes into account the mechanical properties of the arm. Exp Brain Res 124:42–52

    Article  CAS  PubMed  Google Scholar 

  63. Schmitt GJ, Meisenzahl EM, Dresel S, Tatsch K, Rossmuller B, Frodl T, Preuss UW, Hahn K, Möller HJ (2002) Striatal dopamine D2 receptor binding of risperidone in schizophrenic patients as assessed by 123I-iodobenzamide SPECT: a comparative study with olanzapine. J Psychopharmacol 16:200–206

    Article  CAS  PubMed  Google Scholar 

  64. Sweeney JA, Mintun MA, Kwee S, Wiseman MB, Brown DL, Rosenberg DR, Carl JR (1996) Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J Neurophysiol 75:454–468

    CAS  PubMed  Google Scholar 

  65. Thaker GK, Nguyen JA, Tamminga CA (1989) Saccadic distractibility in schizophrenic patients with tardive dyskinesia. Arch Gen Psychiat 46(8):755–756

    CAS  PubMed  Google Scholar 

  66. Tigges P, Mergl R, Frodl T, Meisenzahl EM, Gallinat J, Schröter A, Riedel M, Müller N, Möller HJ, Hegerl U (2000) Digitized analysis of abnormal hand-motor performance in schizophrenic patients. Schizophr Res 45:133–143

    Article  CAS  PubMed  Google Scholar 

  67. Tsujimoto S, Sawaguchi T (2005) Neuronal activity representing temporal prediction of reward in the primate prefrontal cortex. J Neurophysiol 93:3687–3692

    Article  PubMed  Google Scholar 

  68. Vercher JL, Lazzari S, Gauthier G (1997) Manuo-ocular coordination in target tracking. II. Comparing the model with human behavior. Biol Cybern 77:267–275

    Article  CAS  PubMed  Google Scholar 

  69. Wenban-Smith MG, Findlay JM (1991) Express saccades: is there a separate population in humans? Exp Brain Res 87:218–222

    Article  CAS  PubMed  Google Scholar 

  70. Wölwer W, Falkai P, Streit M, Gaebel W (2003) Trait characteristic of impaired visuomotor integration during trail-making test B performance in schizophrenia. Neuropsychobiology 48:59–67

    Article  PubMed  Google Scholar 

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Acknowledgements

This research was supported by the Deutsche Forschungsgemeinschaft (DFG) via SFB 462 “Sensomotorik”, DFG-Grant Str 436/7-1, and a DFG-fellowship to U.S. We thank Roland S. Johansson for helpful suggestions on the analysis of the data.

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Correspondence to Uta Sailer.

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Sailer, U., Eggert, T., Strassnig, M. et al. Predictive eye and hand movements are differentially affected by schizophrenia. Eur Arch Psychiatry Clin Neurosc 257, 413–422 (2007). https://doi.org/10.1007/s00406-007-0749-8

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  • DOI: https://doi.org/10.1007/s00406-007-0749-8

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