Auditory oddball fMRI in schizophrenia: Association of negative symptoms with regional hypoactivation to novel distractors

Brain Imaging and Behavior

Volumn 2, Issue 2, 2008, Pages 132-145

  Wolf, Daniel H ^a   Turetsky, Bruce I ^a   Loughead, James ^a   Elliott, Mark A ^a   Pratiwadi, Ramapriyan ^a   Gur, Raquel E ^a,b   Gur, Ruben C ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Auditory oddball; Deviance detection; Functional MRI; Negative symptoms; Schizophrenia; Ventral striatum

Indexed keywords

ADULT; ARTICLE; BRAIN REGION; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROL GROUP; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; INSULA; MALE; NEGATIVE SYNDROME; OCCIPITAL CORTEX; PHENOTYPE; POSITIVE SYNDROME; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA; STIMULUS RESPONSE; TASK PERFORMANCE; TEMPORAL CORTEX;

EID: 77949658107     PISSN: 19317557     EISSN: 19317565     Source Type: Journal    
DOI: 10.1007/s11682-008-9022-7     Document Type: Article

References (89)

1. Abler, B., Erk, S., & Walter, H. (2007). Human reward system activation is modulated by a single dose of olanzapine in healthy subjects in an event-related, double-blind, placebo-controlled fMRI study. Psychopharmacology, 191(3), 823-833.
2. Amedi, A., Malach, R., & Pascual-Leone, A. (2005). Negative BOLD differentiates visual imagery and perception. Neuron, 48(5), 859-872.
3. Andersson, S., & Bergedalen, A. M. (2002). Cognitive correlates of apathy in traumatic brain injury. Neuropsychiatry, Neuropsychoogy, and Behavioral Neurology, 15(3), 184-191.
4. Andreasen, N. C. (1984a). Scale for the assessment of negative symptoms (SANS). Iowa City: University of Iowa.
5. Andreasen, N. C. (1984b). Scale for the assessment of positive symptoms (SAPS). Iowa City: University of Iowa.
6. Andreasen, N. C., Rezai, K., Alliger, R., Swayze 2nd, V. W., Flaum, M., Kirchner, P., et al. (1992). Hypofrontality in neuroleptic-naive patients and in patients with chronic schizophrenia. Assessment with xenon 133 single-photon emission computed tomography and the Tower of London. Archives of General Psychiatry, 49(12), 943-958.
7. Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2003). General multilevel linear modeling for group analysis in fMRI. Neuroimage, 20(2), 1052-1063.
8. Berridge, K. C., & Robinson, T. E. (1998). What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Research Reviews, 28(3), 309-369.
9. Blasi, G., Goldberg, T. E., Weickert, T., Das, S., Kohn, P., Zoltick, B., et al. (2006). Brain regions underlying response inhibition and interference monitoring and suppression. European Journal of Neuroscience, 23(6), 1658-1664.
10. Braff, D. L. (1993). Information processing and attention dysfunctions in schizophrenia. Schizophrenia Bulletin, 19(2), 233-259.
11. Calhoun, V. D., Adali, T., Pearlson, G. D., & Kiehl, K. A. (2006). Neuronal chronometry of target detection: Fusion of hemodynamic and event-related potential data. Neuroimage, 30(2), 544-553.
12. Callicott, J. H., Bertolino, A., Mattay, V. S., Langheim, F. J., Duyn, J., Coppola, R., et al. (2000). Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cerebral Cortex, 10(11), 1078-1092.
13. Canli, T., Qiu, M., Omura, K., Congdon, E., Haas, B. W., Amin, Z., et al. (2006). Neural correlates of epigenesis. Proceedings of the National Academy of Sciences of the United States of America, 103(43), 16033-16038.
14. Culham, J. C. (2006). Functional neuroimaging: Experimental design and analysis. In R. Cabeza, & A. Kingstone (Eds.), Handbook of functional neuroimaging of cognition (2nd ed.). Cambridge, MA: MIT Press.
15. Daffner, K. R., Mesulam, M. M., Scinto, L. F., Acar, D., Calvo, V., Faust, R., et al. (2000). The central role of the prefrontal cortex in directing attention to novel events. Brain, 123(Pt 5), 927-939.
16. Damoiseaux, J. S., Rombouts, S. A., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M., et al. (2006). Consistent resting-state networks across healthy subjects. Proceedings of the National Academy of Sciences of the United States of America, 103(37), 13848-13853.
17. Epstein, J., Pan, H., Kocsis, J. H., Yang, Y., Butler, T., Chusid, J., et al. (2006). Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. American Journal of Psychiatry, 163(10), 1784-1790.
18. Epstein, J., Stern, E., & Silbersweig, D. (1999). Mesolimbic activity associated with psychosis in schizophrenia. Symptom-specific PET studies. Annals of the New York Academy of Sciences, 877, 562-574.
19. First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (1996). Structured clinical interview for DSM-IV axis I disorders, patient edition (SCID-P), version 2. New York: Biometics Research, New York State Psychiatric Institute.
20. Ford, J. M., Johnson, M. B., Whitfield, S. L., Faustman, W. O., & Mathalon, D. H. (2005). Delayed hemodynamic responses in schizophrenia. Neuroimage, 26(3), 922-931.
21. 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(5), 636-647.
22. Garrity, A. G., Pearlson, G. D., McKiernan, K., Lloyd, D., Kiehl, K. A., & Calhoun, V. D. (2007). Aberrant "default mode" functional connectivity in schizophrenia. American Journal of Psychiatry, 164(3), 450-457.
23. Gray, J. A. (1995). Dopamine release in the nucleus accumbens: The perspective from aberrations of consciousness in schizophrenia. Neuropsychologia, 33(9), 1143-1153.
24. Gray, J. A., Joseph, M. H., Hemsley, D. R., Young, A. M., Warburton, E. C., Boulenguez, P., et al. (1995). The role of mesolimbic dopaminergic and retrohippocampal afferents to the nucleus accumbens in latent inhibition: Implications for schizophrenia. Behavioural Brain Research, 71(1-2), 19-31.
25. Green, M. F. (1996). What are the functional consequences of neurocognitive deficits in schizophrenia? American Journal of Psychiatry, 153(3), 321-330.
26. Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 100(1), 253-258.
27. Grillon, C., Courchesne, E., Ameli, R., Geyer, M. A., & Braff, D. L. (1990). Increased distractibility in schizophrenic patients. Electrophysiologic and behavioral evidence. Archives of General Psychiatry, 47(2), 171-179.
28. Gur, R. C., Turetsky, B. I., Loughead, J., Waxman, J., Snyder, W., Ragland, J. D., et al. (2007a). Hemodynamic responses in neural circuitries for detection of visual target and novelty: An event-related fMRI study. Human Brain Mapping, 28(4), 263-274.
29. Gur, R. E., Turetsky, B. I., Loughead, J., Snyder, W., Kohler, C., Elliott, M., et al. (2007b). Visual attention circuitry in schizophrenia investigated with oddball event-related functional magnetic resonance imaging. American Journal of Psychiatry, 164(3), 442-449.
30. Harris, J. G., Minassian, A., & Perry, W. (2007). Stability of attention deficits in schizophrenia. Schizophrenia Research, 91(1-3), 107-111.
31. Harrison, B. J., Yucel, M., Pujol, J., & Pantelis, C. (2007). Task-induced deactivation of midline cortical regions in schizophrenia assessed with fMRI. Schizophrenia Research, 91(1-3), 82-86.
32. Ho, B. C., Andreasen, N. C., Nopoulos, P., Arndt, S., Magnotta, V., & Flaum, M. (2003). Progressive structural brain abnormalities and their relationship to clinical outcome: A longitudinal magnetic resonance imaging study early in schizophrenia. Archives of General Psychiatry, 60(6), 585-594.
33. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage, 17(2), 825-841.
34. Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2), 143-156.
35. Jensen, J., Smith, A. J., Willeit, M., Crawley, A. P., Mikulis, D. J., Vitcu, I., et al. (2007). Separate brain regions code for salience vs. valence during reward prediction in humans. Human Brain Mapping, 28(4), 294-302.
36. Jezzard, P., & Balaban, R. S. (1995). Correction for geometric distortion in echo planar images from B0 field variations. Magnetic Resonance in Medicine, 34(1), 65-73.
37. Juckel, G., Schlagenhauf, F., Koslowski, M., Filonov, D., Wustenberg, T., Villringer, A., et al. (2006a). Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology (Berlin), 187(2), 222-228.
38. Juckel, G., Schlagenhauf, F., Koslowski, M., Wustenberg, T., Villringer, A., Knutson, B., et al. (2006b). Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage, 29(2), 409-416.
39. Kapur, S. (2003). Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia. American Journal of Psychiatry, 160(1), 13-23.
40. Katayama, J., & Polich, J. (1999). Auditory and visual P300 topography from a 3 stimulus paradigm. Clinical Neurophysiology, 110(3), 463-468.
41. Keedwell, P. A., Andrew, C., Williams, S. C., Brammer, M. J., & Phillips, M. L. (2005). The neural correlates of anhedonia in major depressive disorder. Biological Psychiatry, 58(11), 843-853.
42. Kiehl, K. A., Laurens, K. R., Duty, T. L., Forster, B. B., & Liddle, P. F. (2001). Neural sources involved in auditory target detection and novelty processing: An event-related fMRI study. Psychophysiology, 38(1), 133-142.
43. Kiehl, K. A., & Liddle, P. F. (2001). An event-related functional magnetic resonance imaging study of an auditory oddball task in schizophrenia. Schizophrenia Research, 48(2-3), 159-171.
44. Kiehl, K. A., Stevens, M. C., Celone, K., Kurtz, M., & Krystal, J. H. (2005a). Abnormal hemodynamics in schizophrenia during an auditory oddball task. Biological Psychiatry, 57(9), 1029-1040.
45. Kiehl, K. A., Stevens, M. C., Laurens, K. R., Pearlson, G., Calhoun, V. D., & Liddle, P. F. (2005b). An adaptive reflexive processing model of neurocognitive function: Supporting evidence from a large scale (n = 100) fMRI study of an auditory oddball task. Neuroimage, 25(3), 899-915.
46. Kuroki, N., Shenton, M. E., Salisbury, D. F., Hirayasu, Y., Onitsuka, T., Ersner-Hershfield, H., et al. (2006). Middle and inferior temporal gyrus gray matter volume abnormalities in first-episode schizophrenia: An MRI study. American Journal of Psychiatry, 163(12), 2103-2110.
47. Laruelle, M., & Abi-Dargham, A. (1999). Dopamine as the wind of the psychotic fire: New evidence from brain imaging studies. Journal of Psychopharmacology, 13(4), 358-371.
48. Laurens, K. R., Kiehl, K. A., Ngan, E. T., & Liddle, P. F. (2005). Attention orienting dysfunction during salient novel stimulus processing in schizophrenia. Schizophrenia Research, 75(2-3), 159-171.
49. Laurienti, P. J., Burdette, J. H., Wallace, M. T., Yen, Y. F., Field, A. S., & Stein, B. E. (2002). Deactivation of sensory-specific cortex by cross-modal stimuli. Journal of Cognitive Neuroscience, 14(3), 420-429.
50. Liddle, P. F., Friston, K. J., Frith, C. D., Hirsch, S. R., Jones, T., & Frackowiak, R. S. (1992). Patterns of cerebral blood flow in schizophrenia. British Journal of Psychiatry, 160, 179-186.
51. Liddle, P. F., Laurens, K. R., Kiehl, K. A., & Ngan, E. T. (2006). Abnormal function of the brain system supporting motivated attention in medicated patients with schizophrenia: An fMRI study. Psychological Medicine, 36(8), 1097-1108.
52. Linden, D. E., Prvulovic, D., Formisano, E., Vollinger, M., Zanella, F. E., Goebel, R., et al. (1999). The functional neuroanatomy of target detection: An fMRI study of visual and auditory oddball tasks. Cerebral Cortex, 9(8), 815-823.
53. Lisman, J. E., & Grace, A. A. (2005). The hippocampal-VTA loop: Controlling the entry of information into long-term memory. Neuron, 46(5), 703-713.
54. Mahurin, R. K., Velligan, D. I., & Miller, A. L. (1998). Executive-frontal lobe cognitive dysfunction in schizophrenia: A symptom subtype analysis. Psychiatry Research, 79(2), 139-149.
55. Mason, M. F., Norton, M. I., van Horn, J. D., Wegner, D. M., Grafton, S. T., & Macrae, C. N. (2007). Wandering minds: The default network and stimulus-independent thought. Science, 315(5810), 393-395.
56. Mathalon, D. H., Ford, J. M., & Pfefferbaum, A. (2000). Trait and state aspects of P300 amplitude reduction in schizophrenia: A retrospective longitudinal study. Biological Psychiatry, 47(5), 434-449.
57. Mathalon, D. H., Heinks, T., & Ford, J. M. (2004). Selective attention in schizophrenia: Sparing and loss of executive control. American Journal of Psychiatry, 161(5), 872-881.
58. McCarthy, G., Luby, M., Gore, J., & Goldman-Rakic, P. (1997). Infrequent events transiently activate human prefrontal and parietal cortex as measured by functional MRI. Journal of Neurophysiology, 77(3), 1630-1634.
59. McClure, M. M., Bowie, C. R., Patterson, T. L., Heaton, R. K., Weaver, C., Anderson, H., et al. (2007). Correlations of functional capacity and neuropsychological performance in older patients with schizophrenia: Evidence for specificity of relationships? Schizophrenia Research, 89(1-3), 330-338.
60. Menon, V., Adleman, N. E., White, C. D., Glover, G. H., & Reiss, A. L. (2001). Error-related brain activation during a Go/NoGo response inhibition task. Human Brain Mapping, 12(3), 131-143.
61. Menon, V., Ford, J. M., Lim, K. O., Glover, G. H., & Pfefferbaum, A. (1997). Combined event-related fMRI and EEG evidence for temporal-parietal cortex activation during target detection. Neuroreport, 8(14), 3029-3037.
62. Menzies, L., Ooi, C., Kamath, S., Suckling, J., McKenna, P., Fletcher, P., et al. (2007). Effects of gamma-aminobutyric acid-modulating drugs on working memory and brain function in patients with schizophrenia. Archives of General Psychiatry, 64(2), 156-167.
63. Morey, R. A., Inan, S., Mitchell, T. V., Perkins, D. O., Lieberman, J. A., & Belger, A. (2005). Imaging frontostriatal function in ultra-high-risk, early, and chronic schizophrenia during executive processing. Archives of General Psychiatry, 62(3), 254-262.
64. Muller-Gass, A., Macdonald, M., Schröger, E., Sculthorpe, L., & Campbell, K. (2007). Evidence for the auditory P3a reflecting an automatic process: Elicitation during highly-focused continuous visual attention. Brain Research, 1170(1), 71-78.
65. Opitz, B., Mecklinger, A., Friederici, A. D., & von Cramon, D. Y. (1999a). The functional neuroanatomy of novelty processing: Integrating ERP and fMRI results. Cerebral Cortex, 9(4), 379-391.
66. Opitz, B., Mecklinger, A., Von Cramon, D. Y., & Kruggel, F. (1999b). Combining electrophysiological and hemodynamic measures of the auditory oddball. Psychophysiology, 36(1), 142-147.
67. Pasley, B. N., Inglis, B. A., & Freeman, R. D. (2007). Analysis of oxygen metabolism implies a neural origin for the negative BOLD response in human visual cortex. Neuroimage, 36(2), 269-276.
68. Pfefferbaum, A., Ford, J. M., White, P. M., & Roth, W. T. (1989). P3 in schizophrenia is affected by stimulus modality, response requirements, medication status, and negative symptoms. Archives of General Psychiatry, 46(11), 1035-1044.
69. Plaze, M., Bartres-Faz, D., Martinot, J., Januel, D., Bellivier, F., De Beaurepaire, R., et al. (2006). Left superior temporal gyrus activation during sentence perception negatively correlates with auditory hallucination severity in schizophrenia patients. Schizophrenia Research, 87, 109-115.
70. Polich, J. (2007). Updating P300: an integrative theory of P3a and P3b. Clinical Neurophysiology, 118(10), 2128-2148.
71. Prouteau, A., Verdoux, H., Briand, C., Lesage, A., Lalonde, P., Nicole, L., et al. (2004). The crucial role of sustained attention in community functioning in outpatients with schizophrenia. Psychiatry Research, 129(2), 171-177.
72. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 676-682.
73. Roth, R. M., Koven, N. S., Pendergrass, J. C., Flashman, L. A., McAllister, T. W., & Saykin, A. J. (2008). Apathy and the processing of novelty in schizophrenia. Schizophrenia Research, 98(1-3), 232-238.
74. Sawaki, R., & Katayama, J. (2007). Difficulty of discrimination modulates attentional capture for deviant information. Psychophysiology, 44(3), 374-382.
75. Schlagenhauf, F., Juckel, G., Koslowski, M., Kahnt, T., Knutson, B., Dembler, T. et al. (2008). Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine. Psychopharmacology, 196(4), 673-684.
76. Shmuel, A., Yacoub, E., Pfeuffer, J., van de Moortele, P. F., Adriany, G., Hu, X., et al. (2002). Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron, 36(6), 1195-1210.
77. Silver, H., & Feldman, P. (2005). Evidence for sustained attention and working memory in schizophrenia sharing a common mechanism. Journal of Neuropsychiatry and Clinical Neurosciences, 17(3), 391-398.
78. Simpson Jr., J. R., Drevets, W. C., Snyder, A. Z., Gusnard, D. A., & Raichle, M. E. (2001). Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 688-693.
79. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143-155.
80. Squires, N. K., Squires, K. C., & Hillyard, S. A. (1975). Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. Electroencephalography and Clinical Neurophysiology, 38(4), 387-401.
81. Stevens, A. A., Skudlarski, P., Gatenby, J. C., & Gore, J. C. (2000). Event-related fMRI of auditory and visual oddball tasks. Magnetic Resonance Imaging, 18(5), 495-502.
82. Taylor, S. F., Phan, K. L., Britton, J. C., & Liberzon, I. (2005). Neural response to emotional salience in schizophrenia. Neuropsychopharmacology, 30(5), 984-995.
83. Turetsky, B. I., Colbath, E. A., & Gur, R. E. (1998a). P300 subcomponent abnormalities in schizophrenia: I. Physiological evidence for gender and subtype specific differences in regional pathology. Biological Psychiatry, 43(2), 84-96.
84. Turetsky, B. I., Colbath, E. A., & Gur, R. E. (1998b). P300 subcomponent abnormalities in schizophrenia: II. Longitudinal stability and relationship to symptom change. Bioogical Psychiatry, 43(1), 31-39.
85. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15(1), 273-289.
86. Woolrich, M. W., Behrens, T. E., Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2004). Multilevel linear modelling for fMRI group analysis using Bayesian inference. Neuroimage, 21(4), 1732-1747.
87. Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of fMRI data. Neuroimage, 14(6), 1370-1386.
88. Zink, C. F., Pagnoni, G., Chappelow, J., Martin-Skurski, M., & Berns, G. S. (2006). Human striatal activation reflects degree of stimulus saliency. Neuroimage, 29(3), 977-983.
89. Zink, C. F., Pagnoni, G., Martin, M. E., Dhamala, M., & Berns, G. S. (2003). Human striatal response to salient nonrewarding stimuli. Journal of Neuroscience, 23(22), 8092-8097.