Anomalous neural circuit function in schizophrenia during a virtual Morris water task

NeuroImage

Volumn 49, Issue 4, 2010, Pages 3373-3384

  Folley, Bradley S ^a,b   Astur, Robert ^a,c   Jagannathan, Kanchana ^a   Calhoun, Vince D ^a,c,d,e   Pearlson, Godfrey D ^a,c  

^a INSTITUTE OF LIVING   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MIND RESEARCH NETWORK   (United States)

^e University of New Mexico   (United States)

Author keywords

Allocentric; fMRI; Hippocampus; Independent component analysis; Morris Water Maze; Spatial learning

Indexed keywords

WATER;

ADULT; ARTICLE; BRAIN DYSFUNCTION; BRAIN FUNCTION; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HIPPOCAMPUS; HUMAN; INDEPENDENT COMPONENT ANALYSIS; LEARNING; LEARNING DISORDER; MAJOR CLINICAL STUDY; MALE; MEMORY DISORDER; MORPHOMETRICS; NEUROANATOMY; PARIETAL LOBE; PRIORITY JOURNAL; SCHIZOPHRENIA; SPATIAL DISCRIMINATION; STRIATE CORTEX; TASK PERFORMANCE; TEMPORAL LOBE; VIRTUAL REALITY;

BRAIN; BRAIN MAPPING; MAGNETIC RESONANCE IMAGING; MAZE LEARNING; NERVE NET; SCHIZOPHRENIA;

EID: 73749086389     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.11.034     Document Type: Article

References (78)

1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders DSM-IV-TR (Text Revision) (2000), American Psychiatric Association Press, Washington, D.C.
2. Amunts K., Kedo O., Kindler M., Pieperhoff P., Mohlberg H., Shah N.J., et al. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat. Embryol. 210 (2005) 343-352
3. Antonova E., Sharma T., Morris R., and Kumari V. The relationship between brain structure and neurocognition in schizophrenia: a selective review. Schizophr. Res. 70 (2004) 117-145
4. Astur R.S., Ortiz M.L., and Sutherland R.J. A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav. Brain Res. 93 (1998) 185-190
5. Astur R.S., Taylor L.B., Mamelak A.N., Philpott L., and Sutherland R.J. Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behav. Brain Res. 132 (2002) 77-84
6. Astur R.S., Tropp J., Sava S., Constable R.T., and Markus E.J. Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behav. Brain Res. 151 (2004) 103-115
7. Astur R., Germain S., Tolin D., Ford J., Russell D., and Stevens M. Hippocampus function predicts severity of post-traumatic stress disorder. CyberPsychol. Behav. 9 (2006) 234-240
8. Benes F.M., Kwok E.W., Vincent S.L., and Todtenkopf M.S. A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol. Psychiatry 44 (1998) 88-97
9. Blair J.R., and Spreen O. Predicting premorbid IQ: a revision of the National Adult Reading Test. Clin. Neuropsychol. 3 (1989) 129-136
10. Broadbent N.J., Squire L.R., and Clark R.E. Reversible hippocampal lesions disrupt water maze performance during both recent and remote memory tests. Learn. Mem. 13 (2006) 187-191
11. Brown R.G., and Pluck G. Negative symptoms: the 'pathology' of motivation and goal-directed behaviour. Trends Neurosci. 23 (2000) 412-417
12. Brown M.A., and Sharp P.E. Simulation of spatial learning in the Morris water maze by a neural network model of the hippocampal formation and nucleus accumbens. Hippocampus 5 (1995) 171-188
13. Calhoun V.D., and Adali T. Unmixing fMRI with independent component analysis. IEEE Eng. Med. Biol. Mag. 25 (2006) 79-90
14. Calhoun V.D., Adali T., McGinty V.B., Pekar J.J., Watson T.D., and Pearlson G.D. fMRI activation in a visual-perception task: network of areas detected using the general linear model and independent components analysis. Neuroimage 14 (2001) 1080-1088
15. Calhoun V.D., Adali T., Pearlson G.D., and Pekar J.J. A method for making group inferences from functional MRI data using independent component analysis. Hum. Brain Mapp. 14 (2001) 140-151
16. Calhoun V.D., Adali T., Hansen L.K., Larsen J., and Pekar J.J. ICA of functional MRI data: an overview. Fourth International Symposium on Independent Component Analysis and Blind Signal Separation (ICA2003), April, Nara, Japan (2003) 281-288
17. Calhoun V.D., Kiehl K.A., Liddle P.F., and Pearlson G.D. Aberrant localization of synchronous hemodynamic activity in auditory cortex reliably characterizes schizophrenia. Biol. Psychiatry 55 (2004) 842-849
18. Calhoun V.D., Pekar J.J., and Pearlson G.D. Alcohol intoxication effects on simulated driving: exploring alcohol-dose effects on brain activation using functional MRI. Neuropsychopharmacology 29 (2004) 2017-2097
19. Carter C., Robertson L., Nordahl T., Chaderjian M., Kraft L., and O'Shora-Celaya L. Spatial working memory pathology and negative symptoms in schizophrenia. Biol. Psychiatry 37 (1995) 637-638
20. Courtney S.M., Petit L., Maisog J.M., Ungerleider L.G., and Haxby J.V. An area specialized for spatial working memory in human frontal cortex. Science (New York, NY. 279 (1998) 1347-1351
21. Crucian G.P., and Berenbaum S.A. Sex differences in right hemisphere tasks. Brain Cogn. 36 (1998) 377-389
22. Czurkó A., Czéh B., Seress L., Nadel L., and Bures J. Severe spatial navigation deficit in the Morris water maze after single high dose of neonatal x-ray irradiation in the rat. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 2766-2771
23. D'Esposito M., Alexander M.P., Fischer R., McGlinchey-Berroth R., and O'Connor M. Recovery of memory and executive function following anterior communicating artery aneurysm rupture. J. Int. Neuropsychol. Soc. 2 (1996) 565-570
24. D'Esposito M., Postle B.R., Ballard D., and Lease J. Maintenance versus manipulation of information held in working memory: an event-related fMRI study. Brain Cogn. 41 (1999) 66-86
25. D'Hooge R., and De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. 36 (2001) 60-90
26. Devan B.D., and White N.M. Parallel information processing in the dorsal striatum: relation to hippocampal function. J. Neurosci. 19 (1999) 2789-2798
27. Devan B.D., Goad E.H., and Petri H.L. Dissociation of hippocampal and striatal contributions to spatial navigation in the water maze. Neurobiol. Learn. Mem. 66 (1996) 305-323
28. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25 (2005) 1325-1335
29. Ekstrom A.D., Kahana M.J., Caplan J.B., Fields T.A., Isham E.A., Newman E.L., et al. Cellular networks underlying human spatial navigation. Nature 425 (2003) 184-188
30. Evans A.C., Collins D.L., Mills S.R., Brown E.D., Kelly R.L., and Peters T.M. 3D statistical neuroanatomical models from 305 MRI volumes. Proceedings of the IEEE Nuclear Science Symposium and Medical Imaging Conference (1993) 1813-1817
31. Fletcher P., McKenna P.J., Friston K.J., Frith C.D., and Dolan R.J. Abnormal cingulate modulation of fronto-temporal connectivity in schizophrenia. Neuroimage 9 (1999) 337-342
32. Freire L., and Mangin J.F. Motion correction algorithms may create spurious brain activations in the absence of subject motion. Neuroimage 14 (2001) 709-722
33. Garrity A.G., Pearlson G.D., McKiernan K., Lloyd D., Kiehl K.A., and Calhoun V.D. Aberrant "default mode" functional connectivity in schizophrenia. Am. J. Psychiatry 164 (2007) 450-457
34. Georges-Francois P., Rolls E.T., and Robertson R.G. Spatial view cells in the primate hippocampus: allocentric view not head direction or eye position or place. Cereb. Cortex 9 (1999) 197-212
35. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., and Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14 (2001) 21-36
36. Hafting T., Fyhn M., Molden S., Moser M.B., and Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 436 (2005) 801-806
37. Hanlon F.M., Weisend M.P., Yeo R.A., Huang M., Lee R.R., Thoma R.J., et al. A specific test of hippocampal deficit in schizophrenia. Behav. Neurosci. 119 (2005) 863-875
38. Hanlon F.M., Weisend M.P., Hamilton D.A., Jones A.P., Thoma R.J., Huang M., et al. Impairment on the hippocampal-dependent virtual Morris water task in schizophrenia. Schizophr. Res. 87 (2006) 67-80
39. Harvey P.D., Howanitz E., Parrella M., White L., Davidson M., Mohs R.C., et al. Symptoms, cognitive functioning, and adaptive skills in geriatric patients with lifelong schizophrenia: a comparison across treatment sites. Am. J. Psychiatry 155 (1998) 1080-1086
40. Heckers S., and Konradi C. Hippocampal neurons in schizophrenia. J. Neural. Trans. 109 (2002) 891-905
41. Heckers S., Rauch S.L., Goff D., Savage C.R., Schacter D.L., Fischman A.J., et al. Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nat. Neurosci. 1 (1998) 318-323
42. Hort J., Laczo J., Vyhnalek M., Bojar M., Bures J., and Vlcek K. Spatial navigation deficit in amnestic mild cognitive impairment. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 4042-4047
43. Kay S.R., Fiszbein A., and Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13 (1987) 261-276
44. Ku J., Cho W., Kim J., Peled A., Wiederhold B.K., Wiederhold M.D., et al. A virtual environment for investigating schizophrenic patients' characteristics: assessment of cognitive and navigation ability. Cyberpsychol. Behav. 6 (2003) 397-404
45. Kubicki M., Westin C.F., Maier S.E., Frumin M., Nestor P.G., Salisbury D.F., et al. Uncinate fasciculus findings in schizophrenia: a magnetic resonance diffusion tensor imaging study. Am. J. Psychiatry 159 (2002) 813-820
46. Lalonde R. Cerebellar contributions to instrumental learning. Neurosci. Biobehav. Rev. 18 (1994) 161-170
47. Livingstone S.A., and Skelton R.W. Virtual environment navigation tasks and the assessment of cognitive deficits in individuals with brain injury. Behav. Brain Res. 185 (2007) 21-31
48. MacDonald III A.W., and Carter C.S. Cognitive experimental approaches to investigating impaired cognition in schizophrenia: a paradigm shift. J. Clin. Exp. Neuropsychol. 24 (2002) 873-882
49. Maguire E.A., Frackowiak R.S., and Frith C.D. Recalling routes around London: activation of the right hippocampus in taxi drivers. J. Neurosci. 17 (1997) 7103-7110
50. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S., Frith C.D., and O'Keefe J. Knowing where and getting there: a human navigation network. Science 280 (1998) 921-924
51. Maguire E.A., Spiers H.J., Good C.D., Hartley T., Frackowiak R.S., and Burgess N. Navigation expertise and the human hippocampus: a structural brain imaging analysis. Hippocampus 13 (2003) 250-259
52. Maldjian J.A., Laurienti P.J., Kraft R.A., and Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19 (2003) 1233-1239
53. Mechelli A., Price C., Friston K., and Ashburner J. Voxel-based morphometry of the human brain: methods and applications. Curr. Med. Imag. Rev. 1 (2005) 105-113
54. Mogensen J., Pedersen T.K., Holm S., and Bang L.E. Prefrontal cortical mediation of rats' place learning in a modified water maze. Brain Res. Bull. 38 (1995) 425-434
55. Morris R.G.M. Spatial localization does not require the presence of local cues. Learn. Motiv. 12 (1981) 239-260
56. Morris R.G.M., Garrud P., Rawlins J., and O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 297 (1982) 681-683
57. Moses S.N., Ryan J.D., Bardouille T., Kovacevic N., Hanlon F.M., and McIntosh A.R. Semantic information alters neural activation during transverse patterning performance. Neuroimage 46 (2009) 863-873
58. Mumby D.G., Cameli L., and Glenn M.J. Impaired allocentric spatial memory and intact retrograde memory after thalamic damage caused by thiamine deficiency in rats. Behav. Neurosci. 113 (1999) 42-50
59. Nakazawa K., McHugh T.J., Wilson M.A., and Tonegawa S. NMDA receptors, place cells and hippocampal spatial memory. Nat. Rev. 5 (2004) 361-372
60. Naqvi N.H., Rudrauf D., Damasio H., and Bechara A. Damage to the insula disrupts addiction to cigarette smoking. Science 315 (2007) 531-534
61. Newhouse P., Newhouse C., and Astur R.S. Sex differences in visual-spatial learning using a virtual water maze in pre-pubertal children. Behav. Brain Res. 183 (2007) 1-7
62. O'Keefe J., and Nadel L. The hippocampus as a cognitive map (1978), Clarendon Press, Oxford
63. O'Keefe J., Nadel L., Keightley S., and Kill D. Fornix lesions selectively abolish place learning in the rat. Exp. Neurol. 48 (1975) 152-166
64. Ortigue S., Grafton S.T., and Bianchi-Demicheli F. Correlation between insula activation and self-reported quality of orgasm in women. Neuroimage 37 (2007) 551-560
65. Pine D.S., Grun J., Maguire E.A., Burgess N., Zarahn E., Koda V., et al. Neurodevelopmental aspects of spatial navigation: a virtual reality fMRI study. Neuroimage 15 (2002) 396-406
66. Ragland J.D., Gur R.C., Raz J., Schroeder L., Kohler C.G., Smith R.J., et al. Effect of schizophrenia on frontotemporal activity during word encoding and recognition: a PET cerebral blood flow study. Am. J. Psychiatry 158 (2001) 1114-1125
67. Rosene D., and van Hoesen G. The hippocampal formation of the primate brain. A review of some comparative aspects of cytoarchitecture and connections. In: Jones E., and Peters A. (Eds). Further aspects of cortical function, including hippocampus (1987), Plenum, New York 345-456
68. Sakai K., Rowe J.B., and Passingham R.E. Active maintenance in prefrontal area 46 creates distractor-resistant memory. Nat. Neurosci. 5 (2002) 479-484
69. Shipman S., and Astur R. Factors affecting the hippocampal BOLD response during spatial memory. Behav. Brain Res. 187 (2008) 433-441
70. Squire L.R. Memory and brain (1987), Oxford Unive. Press, New York; Oxford
71. Stone J.M., Morrison P.D., and Pilowsky L.S. Glutamate and dopamine dysregulation in schizophrenia-a synthesis and selective review. J. Psychopharmacol. 21 (2007) 440-452
72. Sutherland R.J., Whishaw I.Q., and Kolb B. A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat. Behav. Brain Res. 7 (1983) 133-153
73. Szendi I., Kiss M., Racsmany M., Boda K., Cimmer C., Voros E., et al. Correlations between clinical symptoms, working memory functions and structural brain abnormalities in men with schizophrenia. Psychiatry Res. 147 (2006) 47-55
74. Talairach J., and Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System - an Approach to Cerebral Imaging (1988), Thieme Medical Publishers, New York
75. Waite J.J., Chen A.D., Wardlow M.L., and Thal L.J. Behavioral and biochemical consequences of combined lesions of the medial septum/ diagonal band and nucleus basalis in the rat when ibotenic acid, quisqualic acid, and AMPA are used. Exp. Neurol. 130 (1994) 214-229
76. Weniger G., and Irle E. Allocentric memory impaired and egocentric memory intact as assessed by virtual reality in recent-onset schizophrenia. Schizophr. Res. 101 (2008) 201-209
77. Yin H.H., and Knowlton B.J. Contributions of striatal subregions to place and response learning. Learn. Mem. 11 (2004) 459-463
78. Zhang Z.J., and Reynolds G.P. A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr. Res. 55 (2002) 1-10