Egocentric spatial learning in schizophrenia investigated with functional magnetic resonance imaging

NeuroImage: Clinical

Volumn 1, Issue 1, 2012, Pages 153-163

  Siemerkus, Jakob ^a,b   Irle, Eva ^b   Schmidt Samoa, Carsten ^b   Dechent, Peter ^b   Weniger, Godehard ^a  

^a UNIVERSITY HOSPITAL OF PSYCHIATRY   (Switzerland)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Cingulate cortex; Positive symptoms; Precuneus; Retrosplenial cortex; Spatial memory; Virtual reality

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HOSPITAL PATIENT; HUMAN; IMAGE ANALYSIS; LEARNING; MALE; MAZE TEST; PERFORMANCE; POSITIVE SYNDROME; POSTERIOR CINGULATE; PRECUNEUS; PRIORITY JOURNAL; RETROSPLENIAL CORTEX; SCHIZOPHRENIA; SPATIAL LEARNING;

EID: 84871999033     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2012.10.004     Document Type: Article

References (75)

1. Aguirre, G.K., Detre, J.A., Alsop, D.C., D'Esposito, M., 1996. The parahippocampus subserves topographical learning inman. Cerebral Cortex 6, 823-829.
2. Andersen, R.A., Essick, G.K., Siegel, R.M., 1985. Encoding of spatial location by posterior parietal neurons. Science 230, 456-458.
3. Andreasen, N.C., 1983. Scale for the Assessment of Negative Symptoms (SANS). University of Iowa, Iowa City.
4. Andreasen, N.C., 1984. Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa, Iowa City.
5. Andreasen, N.C., O'Leary, D.S., Flaum, M., Nopoulos, P., Watkins, G.L., Boles Ponto, L.L., Hitchwa, R.D., 1997. Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naïve patients. Lancet 349, 1730-1734.
6. Barry, C., Lever, C., Hayman, R., Hartley, T., Burton, S., O'Keefe, J., Jeffery, K., Burgess, N., 2006. The boundary vector cell model of place cell firing and spatial memory. Reviews in the Neurosciences 17, 71-97.
7. Bezchlibnyk-Butler, K.Z., Jeffries, J.J., 2001. Clinical Handbook of Psychotropic Drugs, 11th edition. Hogrefe and Huber, Seattle.
8. Bluhm, R.L., Miller, J., Lanius, R.A., Osuch, E.A., Boksman, K., Neufeld, R.W., Theberge, J., Schaefer, B., Williamson, P., 2007. Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. Schizophrenia Bulletin 33, 1004-1012.
9. Bluhm, R.L., Miller, J., Lanius, R.A., Osuch, E.A., Boksman, K., Neufeld, R.W., Theberge, J., Schaefer, B., Williamson, P., 2009. Retrosplenial cortex connectivity in schizophrenia. Psychiatry Research 174, 17-23.
10. Bohbot, V.D., Iaria, G., Petrides, M., 2004. Hippocampal function and spatial memory, evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology 18, 418-425.
11. Bohbot, V.D., Lerch, J., Thorndycraft, B., Iaria, G., Zijdenbos, A.P., 2007. Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. Journal of Neuroscience 27, 10078-10083.
12. Boynton, G.M., Engel, S.A., Glover, G.H., Heeger, D.J., 1996. Linear systems analysis of functional magnetic resonance imaging in human V1. Journal of Neuroscience 16, 4207-4221.
13. Buckner, R.L., Carroll, D.C., 2007. Self-projection and the brain. Trends in Cognitive Sciences 11, 49-57.
14. Burgess, N., 2006. Spatial memory: how egocentric and allocentric combine. Trends in Cognitive Sciences 10, 551-557.
15. Burgess, N., Maguire, E.A., Spiers, H.J., O'Keefe, J., 2001. A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. NeuroImage 14, 439-453.
16. Cavanna, A.E., Trimble, M.R., 2006. The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564-583.
17. Chapman, L.J., Chapman, J.P., 1973. Problems in the measurement of cognitive deficit. Psychological Bulletin 79, 380-385.
18. Cooke, M.A., Fannon, D., Kulpers, E., Peters, E., Williams, S.C., Kumari, V., 2008. Neurological basis of poor insight in psychosis: a voxel-based MRI study. Schizophrenia Research 103, 40-51.
19. Corlett, P.R., Honey, G.D., Krystal, J.H., Fletcher, P.C., 2011. Glutamatergic model psychosis: prediction error, learning, and inference. Neuropsychopharmacology 36, 294-315.
20. Deakin, J.F.W., Lees, J., McKie, S., Hallak, J.E.C., Williams, S.R., Dursun, S.M., 2008. Glutamate and the neural basis of the subjective effects of ketamine. Archives of General Psychiatry 65, 154-164.
21. Etchamendy, N., Bohbot, V.D., 2007. Spontaneous navigational strategies and performance in the virtual town. Hippocampus 17, 595-599.
22. Etchamendy, N., Konishi, K., Pike, G.B., Marighetto, A., Bohbot, V.D., 2012. Evidence for a virtual human analog of a rodent relational memory task: a study of aging and fMRI in young adults. Hippocampus 22, 869-880.
23. Farrer, C., Frith, C.D., 2002. Experiencing oneself vs another person as being the cause of an action: the neural correlates of the experience of agency. NeuroImage 15, 596-603.
24. 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.
25. Forman, S.D., Cohen, J.D., Fitzgerald, M., Eddy, W.F., Mintun, M.A., Noll, D.C., 1995. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magnetic Resonance in Medicine 33, 636-647.
26. Franck, N., Farrer, C., Georgieff, N.,Marie-Cardine,M., Daléry, J., d'Amato, T., Jeannerod,M., 2001. Defective recognition of one's own actions in patients with schizophrenia. The American Journal of Psychiatry 158, 454-459.
27. Freeman, D., 2008. Studying and treating schizophrenia using virtual reality: a new paradigm. Schizophrenia Bulletin 34, 605-610.
28. Frings, L., Wagner, K., Quiske, A., Schwarzwald, R., Spreer, J., Halsband, U., Schulze-Bonhage, A., 2006. Precuneus is involved in allocentric spatial location encoding and recognition. Experimental Brain Research 173, 661-672.
29. Gardner, D.M., Murphy, L., O'Donnell, H., Detorrino, F., Badessarini, R.J., 2010. International consensus study of antipsychotic dosing. The American Journal of Psychiatry 167, 686-693.
30. Garrity, A.G., Pearlson, G.D., McKiernan, K., Lloyd, D., Kiehl, K.A., Calhoun, V.D., 2007. Aberrant "default mode" functional connectivity in schizophrenia. The American Journal of Psychiatry 164, 450-457.
31. Gusnard, D.A., Raichle, M.E., 2001. Searching for a baseline: functional imaging and the resting human brain. Nature Reviews Neuroscience 2, 685-694.
32. Haaznedar, M.M., Buchsbaum, M.S., Luu, C., Hazlett, E.A., Siegel Jr., B.V., Lohr, J., Wu, J., Haier, R.J., Bunney Jr., W.E., 1997. Decreased anterior cingulate gyrus metabolic rate in schizophrenia. The American Journal of Psychiatry 154, 682-684.
33. Hanlon, F.M., Weisend, M.P., Hamilton, D.A., Jones, A.P., Thoma, R.J., Huang, M., Martin, K., Yeo, R.A., Miller, G.A., Canive, J.M., 2006. Impairment on the hippocampaldependent virtual Morris water task in schizophrenia. Schizophrenia Research 87, 67-80.
34. Härting, C., Markowitsch, H.J., Neufeld, H., Calabrese, P., Deisinger, K., Kessler, J., 2000. WMS-R - Wechsler Gedächtnistest - revidierte Fassung. Huber, Bern.
35. Hassabis, D., Maguire, E.A., 2007. Deconstructing episodic memory with construction. Trends in Cognitive Sciences 11, 299-306.
36. Holdstock, J.S., Mayes, A.R., Cezayirli, E., Isaac, C.L., Aggleton, J.P., Roberts, N., 2000. A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage. Neuropsychologia 38, 410-425.
37. Holt, D.J., Cassidy, B.S., Andrews-Hanna, J.R., Mei Lee, S., Coombs, G., Goff, D.C., Gabrieli, J.D., Moran, J.M., 2011. An anterior-to-posterior shift in midline cortical activity in schizophrenia during self-reflection. Biological Psychiatry 69, 415-423.
38. Honea, R., Crow, T.J., Passingham, D., Mackay, C.E., 2005. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. The American Journal of Psychiatry 162, 2233-2245.
39. Höschel, K., Irle, E., Rüther, E., 1998. Psychopathologic symptoms and cognitive test performance in schizophrenic patients. Fortschritte der Neurologie-Psychiatrie 66, 512-519.
40. Huang, X.Q., Lui, S., Deng, W., Chan, R.C., Wu, Q.Z., Jiang, L.J., Zhang, J.R., Jia, Z.Y., Li, X.L., Li, F., Chen, L., Li, T., Gong, Q.Y., 2010. Localization of cerebral functional deficits in treatment-naïve, first-episode schizophrenia using resting-state fMRI. NeuroImage 49, 2901-2906.
41. Iaria, G., Petrides, M., Dagher, A., Pike, B., Bohbot, V.D., 2003. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. Journal of Neuroscience 23, 5945-5952.
42. Irle, E., Lange, C.,Weniger, G., Sachsse, U., 2007. Size abnormalities of the superior parietal cortices are related to dissociation in borderline personality disorder. Psychiatry Research: Neuroimaging 156, 139-149.
43. Jahn, T., Mussgay, L., 1989. Die statistische Kontrolle möglicher Medikamenteneinflüsse in experimentalpsychologischen Schizophreniestudien: Ein Vorschlag zur Berechnung von Chlorpromazinäquivalenten. Zeitschrift für Klinische Psychologie 18, 257-267.
44. Jang, J.H., Jung, W.H., Choi, J.S., Choi, C.H., Kang, D.H., Shin, N.Y., Hong, K.S., Kwon, J.S., 2011. Reduced prefrontal functional connectivity in the default mode network is related to greater psychopathology in subjects with high genetic loading for schizophrenia. Schizophrenia Research 127, 58-65.
45. King, J.A., Burgess, N., Hartley, T., Vargha-Khadem, F., O'Keefe, J., 2002. Human hippocampus and viewpoint dependence in spatial memory. Hippocampus 12, 811-820.
46. Landgraf, S., Krebs, M.O., Olié, J.P., Committeri, G., van der Meer, E., Berthoz, A., Amado, I., 2010. Real world referencing and schizophrenia: are we experiencing the same reality? Neuropsychologia 48, 2922-2930.
47. Lanius, R.A., Williamson, P.C., Boksman, K., Densmore, M., Gupta, M., Neufeld, R.W., Gati, J.S., Menon, R.S., 2002. Brain activation during script-driven imagery induced dissociative responses in PTSD: a functional magnetic resonance imaging investigation. Biological Psychiatry 52, 305-311.
48. Lui, S., Deng, W., Huang, X., Jiang, L., Ma, X., Chen, H., Zhang, T., Li, X., Li, D., Zou, L., Tang, H., Zhou, X.J., Mechelli, A., Collier, D.A., 2009. Association of cerebral deficits with clinical symptoms in antipsychotic- naïve first-episode schizophrenia: an optimized voxel-based morphometry and resting state functional connectivity study. The American Journal of Psychiatry 166, 196-205.
49. Lui, S., Li, T., Deng, W., Jiang, L., Wu, Q., Tang, H., Yue, Q., Huang, X., Chan, R.C., Collier, D.A., Shashwath, A.M., Pearlson, G., Mechelli, A., Sweeney, J.A., Gong, Q., 2010. Short-term effects of antipsychotic treatment on cerebral function in drug-naïve first-episode schizophrenia revealed by "resting state" functional magnetic resonance imaging. Archives of General Psychiatry 67, 783-792.
50. Maguire, E.A., 2001. The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scandinavian Journal of Psychology 42, 225-238.
51. Maguire, E.A., Burgess, N., Donnett, J.G., Frackowiak, R.S., Frith, C.D., O'Keefe, J., 1998. Knowing where and getting there: a human navigation network. Science 280, 921-924.
52. Moore, J.W., Cambridge, V.C.,Morgan,H., Giorlando, F., Adapa, R., Fletcher, P.C., 2012. Time, action and psychosis: using subjective time to investigate the effects of ketamine on sense of agency, Neuropsychologia. doi 10.1016/j.neuropsychologia.2012.07.005.
53. Morgan, K.D., Dazzan, P., Morgan, C., Lappin, J., Hutchinson, G., Suckling, J., Fearon, P., Jones, P.B., Leff, J., Murray, R.M., David, A.S., 2010. Insight, grey matter and cognitive function in first-onset psychosis. The British Journal of Psychiatry 197, 141-148.
54. Morgan, H.L., Turner, D.C., Corlett, P.R., Absalom, A.R., Adapa, R., Arana, F.S., Pigott, J., Gardner, J., Everitt, J., Haggard, P., Fletcher, P.C., 2011. Exploring the impact of ketamine on the experience of illusory body ownership. Biological Psychiatry 69, 35-41.
55. Neggers, S.F., Van der Lubbe, R.H., Ramsey, N.F., Postma, A., 2006. Interactions between ego- and allocentric neuronal representations of space. NeuroImage 31, 320-331.
56. O'Keefe, J., Nadel, L., 1978. The hippocampus as a cognitive map. Clarendon Press, Oxford.
57. Olney, J.W., Farber, N.B., 1995. Glutamate receptor dysfunction and schizophrenia. Archives of General Psychiatry 52, 998-1007.
58. Pruessner, J.C., Li, L.M., Serles, W., Pruessner, M., Collins, D.L., Kabani, N., Lupien, S., Evans, A.C., 2000. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cerebral Cortex 10, 433-442.
59. Reske, M., Habel, U., Kellermann, T., Backes, V., Jon Shah, N., von Wilmsdorff, M., Gaebel, W., Zilles, K., Schneider, F., 2009. Differential brain activation during facial emotion discrimination in first-episode schizophrenia. Journal of Psychiatric Research 43, 592-599.
60. Ruby, P., Decety, J., 2001. Effect of subjective perspective taking during simulation of action: a PET investigation of agency. Nature Neuroscience 4, 546-550.
61. Sambataro, F., Blasi, G., Fazio, L., Caforio, G., Taurisano, P., Romano, R., Di Giorgio, A., Gelao, B., Lo Bianco, L., Papazacharias, A., Popolizio, R., Cardini, M., Bertolino, A., 2010. Treatment with olanzapine is associated with modulation of the default mode network in patients with schizophrenia. Neuropsychopharmacology 35, 904-912.
62. Shenton, M.E., Dickey, C.C., Frumin, M., McCarley, R.W., 2001. A review of MRI findings in schizophrenia. Schizophrenia Research 49, 1-52.
63. Spiers, H.J., Maguire, E.A., 2007. A navigational guidance system in the human brain. Hippocampus 17, 618-626.
64. Tewes, U., 1991. HAWIE-R, Hamburg-Wechsler-Intelligenztest für Erwachsene, Revision 1991. Huber, Bern.
65. Waters, F.A., Badcock, J.C., 2010. First-rank symptoms in schizophrenia: reexamining mechanisms of self-recognition. Schizophrenia Bulletin 36, 510-517.
66. Weniger, G., Irle, E., 2006. Posterior parahippocampal gyrus lesions in the human impair egocentric learning in a virtual environment. European Journal of Neuroscience 24, 2406-2414.
67. Weniger, G., Irle, E., 2008. Allocentric memory impaired and egocentricmemory intact as assessed by virtual reality in recent-onset schizophrenia. Schizophrenia Research 101, 201-209.
68. Weniger, G., Ruhleder, M., Wolf, S., Lange, C., Irle, E., 2009. Egocentric memory impaired and allocentric memory intact as assessed by virtual reality in subjects with unilateral parietal cortex lesions. Neuropsychologia 47, 59-69.
69. Weniger, G., Siemerkus, J., Schmidt-Samoa, C., Mehlitz, M., Baudewig, J., Dechent, P., Irle, E., 2010. The human parahippocampal cortex subserves egocentric spatial learning during navigation in a virtual maze. Neurobiology of Learning and Memory 93, 46-55.
70. Weniger, G., Ruhleder, M., Lange, C., Wolf, S., Irle, E., 2011. Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild cognitive impairment. Neuropsychologia 49, 518-527.
71. Weniger, G., Ruhleder, M., Lange, C., Irle, E., 2012. Impaired egocentric memory and reduced somatosensory cortex size in temporal lobe epilepsy with hippocampal sclerosis. Behavioural Brain Research 227, 116-124.
72. Wittchen, H.U., Wunderlich, U., Gruschwitz, S., Zaudig, M., 1997. Strukturiertes Klinisches Interview für DSM-IV (SKID). Hogrefe, Göttingen.
73. Wolbers, T., Büchel, C., 2005. Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. Journal of Neuroscience 25, 3333-3340.
74. Woods, S.D., 2003. Chlorpromazine equivalent doses for the newer atypical antipsychotics. The Journal of Clinical Psychiatry 664, 663-667.
75. Wright, I.C., Rabe-Hesketh, S., Woodruff, P.W.R., David, A.S., Murray, R.M., Bullmore, E.T., 2000. Meta-analysis of regional brain volumes in schizophrenia. The American Journal of Psychiatry 157, 16-25.