A virtual reality task based on animal research - spatial learning and memory in patients after the first episode of schizophrenia

. 2014 ; 8 () : 157. [epub] 20140527

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid24904329

OBJECTIVES: Cognitive deficit is considered to be a characteristic feature of schizophrenia disorder. A similar cognitive dysfunction was demonstrated in animal models of schizophrenia. However, the poor comparability of methods used to assess cognition in animals and humans could be responsible for low predictive validity of current animal models. In order to assess spatial abilities in schizophrenia and compare our results with the data obtained in animal models, we designed a virtual analog of the Morris water maze (MWM), the virtual Four Goals Navigation (vFGN) task. METHODS: Twenty-nine patients after the first psychotic episode with schizophrenia symptoms and a matched group of healthy volunteers performed the vFGN task. They were required to find and remember four hidden goal positions in an enclosed virtual arena. The task consisted of two parts. The Reference memory (RM) session with a stable goal position was designed to test spatial learning. The Delayed-matching-to-place (DMP) session presented a modified working memory protocol designed to test the ability to remember a sequence of three hidden goal positions. RESULTS: Data obtained in the RM session show impaired spatial learning in schizophrenia patients compared to the healthy controls in pointing and navigation accuracy. The DMP session showed impaired spatial memory in schizophrenia during the recall of spatial sequence and a similar deficit in spatial bias in the probe trials. The pointing accuracy and the quadrant preference showed higher sensitivity toward the cognitive deficit than the navigation accuracy. Direct navigation to the goal was affected by sex and age of the tested subjects. The age affected spatial performance only in healthy controls. CONCLUSIONS: Despite some limitations of the study, our results correspond well with the previous studies in animal models of schizophrenia and support the decline of spatial cognition in schizophrenia, indicating the usefulness of the vFGN task in comparative research.

Zobrazit více v PubMed

Addington J., Addington D., Maticka-Tyndale E. (1991). Cognitive functioning and positive and negative symptoms in schizophrenia. Schizophr. Res. 5, 123–134 10.1016/0920-9964(91)90039-T PubMed DOI

Andreasen N. C. (1999). A unitary model of schizophrenia: bleuler's fragmented phrene as schizencephaly. Arch. Gen. Psychiatry 56, 781–787 10.1001/archpsyc.56.9.781 PubMed DOI

Andreasen N. C., Pressler M., Nopoulos P., Miller D., Ho B. C. (2010). Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biol. Psychiatry 67, 255–262 10.1016/j.biopsych.2009.08.040 PubMed DOI PMC

Astur R. S., Ortiz M. L., Sutherland R. J. (1998). A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav. Brain Res. 93, 185–190 10.1016/S0166-4328(98)00019-9 PubMed DOI

Astur R. S., Taylor L. B., Mamelak A. N., Philpott L., Sutherland R. J. (2002). Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behav. Brain Res. 132, 77–84 10.1016/S0166-4328(01)00399-0 PubMed DOI

Astur R. S., Tropp J., Sava S., Constable R. T., Markus E. J. (2004). Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behav. Brain Res. 151, 103–115 10.1016/j.bbr.2003.08.024 PubMed DOI

Barnes T. R., Leeson V. C., Mutsatsa S. H., Watt H. C., Hutton S. B., Joyce E. M. (2008). Duration of untreated psychosis and social function: 1-year follow-up study of first-episode schizophrenia. Br. J. Psychiatry 193, 203–209 10.1192/bjp.bp.108.049718 PubMed DOI PMC

Bohbot V. D., Kalina M., Stepankova K., Spackova N., Petrides M., Nadel L. (1998). Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia 36, 1217–1238 10.1016/S0028-3932(97)00161-9 PubMed DOI

Bubenikova V., Votava M., Horacek J., Palenicek T., Dockery C. (2005). The effect of zotepine, risperidone, clozapine and olanzapine on MK-801-disrupted sensorimotor gating. Pharmacol. Biochem. Behav. 80, 591–596 10.1016/j.pbb.2005.01.012 PubMed DOI

Bubenikova-Valesova V., Horacek J., Vrajova M., Hoschl C. (2008). Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci. Biobehav. Rev. 32, 1014–1023 10.1016/j.neubiorev.2008.03.012 PubMed DOI

Cimadevilla J. M., Fenton A. A., Bures J. (2000). Continuous place avoidance task reveals differences in spatial navigation in male and female rats. Behav. Brain Res. 107, 161–169 10.1016/S0166-4328(99)00128-X PubMed DOI

de Vignemont F., Zalla T., Posada A., Louvegnez A., Koenig O., Georgieff N., et al. (2006). Mental rotation in schizophrenia. Conscious. Cogn. 15, 295–309 10.1016/j.concog.2005.08.001 PubMed DOI

D'Hooge R., De Deyn P. P. (2001). Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 36, 60–90 10.1016/S0165-0173(01)00067-4 PubMed DOI

Dudchenko P. A. (2004). An overview of the tasks used to test working memory in rodents. Neurosci. Biobehav. Rev. 28, 699–709 10.1016/j.neubiorev.2004.09.002 PubMed DOI

Elvevag B., Goldberg T. E. (2000). Cognitive impairment in schizophrenia is the core of the disorder. Crit. Rev. Neurobiol. 14, 1–21 10.1615/CritRevNeurobiol.v14.i1.10 PubMed DOI

Entlerova M., Lobellova V., Hatalova H., Zemanova A., Vales K., Stuchlik A. (2013). Comparison of Long-Evans and Wistar rats in sensitivity to central cholinergic blockade with scopolamine in two spatial tasks: an active place avoidance and the Morris water maze. Physiol. Behav. 120, 11–18 10.1016/j.physbeh.2013.06.024 PubMed DOI

Fischer M. H. (2001). Probing spatial working memory with the Corsi Blocks task. Brain Cogn. 45, 143–154 10.1006/brcg.2000.1221 PubMed DOI

Folley B. S., Astur R., Jagannathan K., Calhoun V. D., Pearlson G. D. (2010). Anomalous neural circuit function in schizophrenia during a virtual Morris water task. Neuroimage 49, 3373–3384 10.1016/j.neuroimage.2009.11.034 PubMed DOI PMC

Garthe A., Behr J., Kempermann G. (2009). Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE 4:e5464 10.1371/journal.pone.0005464 PubMed DOI PMC

Goodrich-Hunsaker N. J., Livingstone S. A., Skelton R. W., Hopkins R. O. (2009). Spatial deficits in a virtual water maze in amnesic participants with hippocampal damage. Hippocampus 119, 1307–1315 10.1002/hipo.20651 PubMed DOI

Gorter J. A., de Bruin J. P. (1992). Chronic neonatal MK-801 treatment results in an impairment of spatial learning in the adult rat. Brain Res. 580, 12–17 10.1016/0006-8993(92)90921-U PubMed DOI

Green M. F., Kern R. S., Heaton R. K. (2004). Longitudinal studies of cognition and functional outcome in schizophrenia: implications for MATRICS. Schizophr. Res. 72, 41–51 10.1016/j.schres.2004.09.009 PubMed DOI

Hamilton D. A., Akers K. G., Johnson T. E., Rice J. P., Candelaria F. T., Sutherland R. J., et al. (2008). The relative influence of place and direction in the Morris water task. J. Exp. Psychol. Anim. Behav. Process. 34, 31–53 10.1037/0097-7403.34.1.31 PubMed DOI

Hanlon F. M., Weisend M. P., Hamilton D. A., Jones A. P., Thoma R. J., Huang M., et al. (2006). Impairment on the hippocampal-dependent virtual Morris water task in schizophrenia. Schizophr. Res. 87, 67–80 10.1016/j.schres.2006.05.021 PubMed DOI

Jacobs L. F., Thomas K. G. F., Laurance H. E., Nadel L. (1998). Place learning in virtual space II: topographical relations as one dimension of stimulus control. Learn. Motiv. 29, 288–308 10.1006/lmot.1998.1008 DOI

Jonasson Z. (2005). Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci. Biobehav. Rev. 28, 811–825 10.1016/j.neubiorev.2004.10.006 PubMed DOI

Jones S. H., Thornicroft G., Coffey M., Dunn G. (1995). A brief mental health outcome scale-reliability and validity of the Global Assessment of Functioning (GAF). Br. J. Psychiatry 166, 654–659 10.1192/bjp.166.5.654 PubMed DOI

Kay S. R., Fiszbein A., Opler L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13, 261–276 10.1093/schbul/13.2.261 PubMed DOI

Keefe R. S., Eesley C. E., Poe M. P. (2005). Defining a cognitive function decrement in schizophrenia. Biol. Psychiatry 57, 688–691 10.1016/j.biopsych.2005.01.003 PubMed DOI

Laczo J., Andel R., Vyhnalek M., Vlcek K., Magerova H., Varjassyova A., et al. (2010). Human analogue of the Morris water maze for testing subjects at risk of Alzheimer's disease. Neurodegener. Dis. 7, 148–152 10.1159/000289226 PubMed DOI

Landgraf S., Krebs M. O., Olie J. P., Committeri G., van der M. E., Berthoz A., et al. (2010). Real world referencing and schizophrenia: are we experiencing the same reality? Neuropsychologia 48, 2922–2930 10.1016/j.neuropsychologia.2010.05.034 PubMed DOI

Latysheva N. V., Rayevsky K. S. (2003). Chronic neonatal N-methyl-D-aspartate receptor blockade induces learning deficits and transient hypoactivity in young rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 27, 787–794 10.1016/S0278-5846(03)00110-6 PubMed DOI

Leplow B., Lehnung M., Pohl J., Herzog A., Ferstl R., Mehdorn M. (2003). Navigational place learning in children and young adults as assessed with a standardized locomotor search task. Br. J. Psychol. 94, 299–317 10.1348/000712603767876244 PubMed DOI

Lipp H. P., Stagliar-Bozicevic M., Fischer M., Wolfer D. P. (1998). A 2-year longitudinal study of swimming navigation in mice devoid of the prion protein: no evidence for neurological anomalies or spatial learning impairments. Behav. Brain Res. 95, 47–54 10.1016/S0166-4328(97)00209-X PubMed DOI

Lobellova V., Entlerova M., Svojanovska B., Hatalova H., Prokopova I., Petrasek T., et al. (2013). Two learning tasks provide evidence for disrupted behavioural flexibility in an animal model of schizophrenia-like behaviour induced by acute MK-801: a dose-response study. Behav. Brain Res. 246, 55–62 10.1016/j.bbr.2013.03.006 PubMed DOI

Marshall M., Lewis S., Lockwood A., Drake R., Jones P., Croudace T. (2005). Association between duration of untreated psychosis and outcome in cohorts of first-episode patients: a systematic review. Arch. Gen. Psychiatry 62, 975–983 10.1001/archpsyc.62.9.975 PubMed DOI

Meltzer H. Y., McGurk S. R. (1999). The effects of clozapine, risperidone, and olanzapine on cognitive function in schizophrenia. Schizophr. Bull. 25, 233–255 10.1093/oxfordjournals.schbul.a033376 PubMed DOI

Meyers J. E., Meyers K. R. (1995). Rey Complex Figure Test and Recognition Trial. Lutz, FL: Psychological Assessment Resources

Moffat S. D. (2009). Aging and spatial navigation: what do we know and where do we go? Neuropsychol. Rev. 19, 478–489 10.1007/s11065-009-9120-3 PubMed DOI

Moffat S. D., Resnick S. M. (2002). Effects of age on virtual environment place navigation and allocentric cognitive mapping. Behav. Neurosci. 116, 851–859 10.1037/0735-7044.116.5.851 PubMed DOI

Morris R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47–60 10.1016/0165-0270(84)90007-4 PubMed DOI

Morris R. G., Garrud P., Rawlins J. N., O'Keefe J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681–683 10.1038/297681a0 PubMed DOI

Morris R. G., Hagan J. J., Rawlins J. N. (1986). Allocentric spatial learning by hippocampectomised rats: a further test of the spatial mapping and working memory theories of hippocampal function. Q. J. Exp. Psychol. B 38, 365–395 PubMed

Morris R. G., Schenk F., Tweedie F., Jarrard L. E. (1990). Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning. Eur. J. Neurosci. 2, 1016–1028 10.1111/j.1460-9568.1990.tb00014.x PubMed DOI

Morris R. G. M. (1981). Spatial localization does not require the presence of local cues. Learn. Motiv. 12, 239–261 10.1016/0023-9690(81)90020-5 DOI

Morris R. G. M. (2008). Morris water maze. Scholarpedia 3:6315 10.4249/scholarpedia.6315 DOI

Mueller S. C., Jackson C. P., Skelton R. W. (2008). Sex differences in a virtual water maze: an eye tracking and pupillometry study. Behav. Brain Res. 193, 209–215 10.1016/j.bbr.2008.05.017 PubMed DOI

Mulder G. B., Pritchett K. (2003). The Morris water maze. Contemp. Top. Lab. Anim. Sci. 42, 49–50 PubMed

Nadel L., Thomas K. G. F., Laurance H. E., Skelton R., Tal T., Jacobs W. J. (1998). Human place learning in a computer generated arena. Lect. Notes Comput. Sci. 1404, 399–428 10.1007/3-540-69342-4_19 PubMed DOI

Norris C. M., Foster T. C. (1999). MK-801 improves retention in aged rats: implications for altered neural plasticity in age-related memory deficits. Neurobiol. Learn. Mem. 71, 194–206 10.1006/nlme.1998.3864 PubMed DOI

O'Carroll C. M., Martin S. J., Sandin J., Frenguelli B., Morris R. G. (2006). Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory. Learn. Mem. 13, 760–769 10.1101/lm.321006 PubMed DOI PMC

Overman W. H., Pate B. J., Moore K., Peuster A. (1996). Ontogeny of place learning in children as measured in the radial arm maze, Morris search task, and open field task. Behav. Neurosci. 110, 1205–1228 10.1037/0735-7044.110.6.1205 PubMed DOI

PEBL. (2012). The Psychology Experiment Building Language. (Version 0.12, Test Battery 0.7). Michigan Technological University; Available online at: http://pebl.sourceforge.net/battery.html

Piskulic D., Olver J. S., Norman T. R., Maruff P. (2007). Behavioural studies of spatial working memory dysfunction in schizophrenia: a quantitative literature review. Psychiatry Res. 150, 111–121 10.1016/j.psychres.2006.03.018 PubMed DOI

Pratt J., Winchester C., Dawson N., Morris B. (2012). Advancing schizophrenia drug discovery: optimizing rodent models to bridge the translational gap. Nat. Rev. Drug Discov. 11, 560–579 10.1038/nrd3649 PubMed DOI

Preiss M. (1997). Trail Making test Pro Děti a Dospělé. Manuál. Bratislava: Psychodiagnostika

Rajji T. K., Ismail Z., Mulsant B. H. (2009). Age at onset and cognition in schizophrenia: meta-analysis. Br. J. Psychiatry 195, 286–293 10.1192/bjp.bp.108.060723 PubMed DOI

Reichenberg A., Harvey P. D., Bowie C. R., Mojtabai R., Rabinowitz J., Heaton R. K., et al. (2009). Neuropsychological function and dysfunction in schizophrenia and psychotic affective disorders. Schizophr. Bull. 35, 1022–1029 10.1093/schbul/sbn044 PubMed DOI PMC

Reitan R. M., Wolfson D. (1993). The Halstead-Reitan Neuropsychological Test battery: Theory and Clinical Interpretation. 2nd edn Tuscon, AZ: Neuropsychology Press

Rodriguez P. F. (2010). Human navigation that requires calculating heading vectors recruits parietal cortex in a virtual and visually sparse water maze task in fMRI. Behav. Neurosci. 124, 532–540 10.1037/a0020231 PubMed DOI

Roof R. L., Stein D. G. (1999). Gender differences in Morris water maze performance depend on task parameters. Physiol Behav. 68, 81–86 10.1016/S0031-9384(99)00162-6 PubMed DOI

Rossi A., Mancini F., Stratta P., Mattei P., Gismondi R., Pozzi F., et al. (1997). Risperidone, negative symptoms and cognitive deficit in schizophrenia: an open study. Acta Psychiatr. Scand. 95, 40–43 10.1111/j.1600-0447.1997.tb00371.x PubMed DOI

Saab B. J., Luca R. M., Yuen W. B., Saab A. M., Roder J. C. (2011). Memantine affects cognitive flexibility in the Morris water maze. J. Alzheimers. Dis. 27, 477–482 10.3233/JAD-2011-110650 PubMed DOI

Sircar R. (2003). Postnatal phencyclidine-induced deficit in adult water maze performance is associated with N-methyl-D-aspartate receptor upregulation. Int. J. Dev. Neurosci. 21, 159–167 10.1016/S0736-5748(03)00026-1 PubMed DOI

Skolimowska J., Wesierska M., Lewandowska M., Szymaszek A., Szelag E. (2011). Divergent effects of age on performance in spatial associative learning and real idiothetic memory in humans. Behav. Brain Res. 218, 87–93 10.1016/j.bbr.2010.11.035 PubMed DOI

Spohn H. E., Strauss M. E. (1989). Relation of neuroleptic and anticholinergic medication to cognitive functions in schizophrenia. J. Abnorm. Psychol. 98, 367–380 10.1037/0021-843X.98.4.367 PubMed DOI

Steele R. J., Morris R. G. (1999). Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus 9, 118–136 PubMed

Stepankova K., Pastalkova E., Kalova E., Kalina M., Bures J. (2003). A battery of tests for quantitative examination of idiothetic and allothetic place navigation modes in humans. Behav. Brain Res. 147, 95–105 10.1016/S0166-4328(03)00141-4 PubMed DOI

Stepankova K., Pastalkova E., Kaminsky Y., Fenton A. A., Bures J. (1999). Allothetic and idiothetic navigation in healthy young humans. Physiol. Res. 48, 123 PubMed

Stuchlik A., Rezacova L., Vales K., Bubenikova V., Kubik S. (2004). Application of a novel Active Allothetic Place Avoidance task (AAPA) in testing a pharmacological model of psychosis in rats: comparison with the Morris Water Maze. Neurosci. Lett. 366, 162–166 10.1016/j.neulet.2004.05.037 PubMed DOI

Šupalová I. (2009). Orientace v Prostoru Zkoumaná ve Virtuální Realitě. (Adaptation Of Spatial Navigation Tests To Virtual Reality). Charles University in Prague

Sutherland R. J., Whishaw I. Q., Kolb B. (1983). A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat. Behav. Brain Res. 7, 133–153 10.1016/0166-4328(83)90188-2 PubMed DOI

Vales K., Bubenikova-Valesova V., Klement D., Stuchlik A. (2006). Analysis of sensitivity to MK-801 treatment in a novel active allothetic place avoidance task and in the working memory version of the Morris water maze reveals differences between Long-Evans and Wistar rats. Neurosci. Res. 55, 383–388 10.1016/j.neures.2006.04.007 PubMed DOI

van der Staay F. J., Rutten K., Erb C., Blokland A. (2011). Effects of the cognition impairer MK-801 on learning and memory in mice and rats. Behav. Brain Res. 220, 215–229 10.1016/j.bbr.2011.01.052 PubMed DOI

Vorhees C. V., Williams M. T. (2006). Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 1, 848–858 10.1038/nprot.2006.116 PubMed DOI PMC

Waller D., Knapp D., Hunt E. (2001). Spatial representations of virtual mazes: the role of visual fidelity and individual differences. Hum. Factors. 43, 147–158 10.1518/001872001775992561 PubMed DOI

Watson D. J., Stanton M. E. (2009). Intrahippocampal administration of an NMDA-receptor antagonist impairs spatial discrimination reversal learning in weanling rats. Neurobiol. Learn. Mem. 92, 89–98 10.1016/j.nlm.2009.02.005 PubMed DOI PMC

Wechsler D. (1997a). Wechsler Adult Intelligence Scale-III San Antonio, TX: The Psychological Corporation; Czech translation by Hogrefe–Testcentrum, Praha 2010.

Wechsler D. (1997b). Manual for the Wechsler Memory Scale-III. San Antonio, TX: Psychological Corporation; Czech translation by Psychodiagnostika, Bratislava: 1999.

Weniger G., Irle E. (2008). Allocentric memory impaired and egocentric memory intact as assessed by virtual reality in recent-onset schizophrenia. Schizophr. Res. 101, 201–209 10.1016/j.schres.2008.01.011 PubMed DOI

Whishaw I. Q. (1991). Latent learning in a swimming pool place task by rats: evidence for the use of associative and not cognitive mapping processes. Q. J. Exp. Psychol. B 43, 83–103 PubMed

Woods S. W. (2003). Chlorpromazine equivalent doses for the newer atypical antipsychotics. J. Clin. Psychiatry 64, 663–667 10.4088/JCP.v64n0607 PubMed DOI

Zemanova A., Stankova A., Lobellova V., Svoboda J., Vales K., Vlcek K., et al. (2013). Visuospatial working memory is impaired in an animal model of schizophrenia induced by acute MK-801: an effect of pretraining. Pharmacol. Biochem. Behav. 106, 117–123 10.1016/j.pbb.2013.03.014 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...