Brain activation patterns during visual episodic memory processing among first-degree relatives of schizophrenia subjects

NeuroImage

Volumn 63, Issue 3, 2012, Pages 1154-1161

  Stolz, Erin ^a   Pancholi, Krishna M ^b   Goradia, Dhruman D ^c   Paul, Sarah ^d   Keshavan, Matcheri S ^e   Nimgaonkar, Vishwajit L ^b   Prasad, Konasale M ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DUQUESNE UNIVERSITY   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cognition; Cognitive neuroscience; Episodic memory; Functional neuroimaging; Schizophrenia

Indexed keywords

ACCURACY; ADULT; ARTICLE; BEHAVIOR; BOLD SIGNAL; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; EPISODIC MEMORY; FAMILY HISTORY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC RISK; HUMAN; INSULA; MAJOR CLINICAL STUDY; MALE; MEMORY DISORDER; MENTAL PERFORMANCE; MENTAL TASK; PREFRONTAL CORTEX; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RECALL; RELATIVE; RESPONSE TIME; SCHIZOPHRENIA; TASK PERFORMANCE; THALAMUS; VISUAL MEMORY;

ADULT; BRAIN; BRAIN MAPPING; FAMILY; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, EPISODIC; PEDIGREE; PHENOTYPE; PHOTIC STIMULATION; REACTION TIME; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84866141326     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.08.030     Document Type: Article

References (75)

1. Achim A.M., Lepage M. Dorsolateral prefrontal cortex involvement in memory post-retrieval monitoring revealed in both item and associative recognition tests. Neuroimage 2005, 24:1113-1121.
2. Achim A.M., Lepage M. Episodic memory-related activation in schizophrenia: meta-analysis. Br. J. Psychiatry 2005, 187:500-509.
3. Aleman A., Hijman R., de Haan E.H.F., Kahn R.S. Memory impairment in schizophrenia: a meta-analysis. Am. J. Psychiatry 1999, 156:1358-1366.
4. Braff D., Schork N.J., Gottesman I.I. Endophenotyping schizophrenia. Am. J. Psychiatry 2007, 164:705-707.
5. Brebion G., Amador X., Smith M.J., Gorman J.M. Mechanisms underlying memory impairment in schizophrenia. Psychol. Med. 1997, 27:383-393.
6. Buckner R.L., Koutstaal W., Schacter D.L., Wagner A.D., Rosen B.R. Functional-anatomic study of episodic retrieval using fMRI. I. Retrieval effort versus retrieval success. Neuroimage 1998, 7:151-162.
7. Buckner R.L., Kelley W.M., Petersen S.E. Frontal cortex contributes to human memory formation. Nat. Neurosci. 1999, 2:311-314.
8. Buzsaki G. The brain's default state: self-organized oscillations in rest and sleep. Rhythms of the Brain 2006, 175-205. Oxford University Press, New York. G. Buzsaki (Ed.).
9. Cabeza R., Dolcos F., Graham R., Nyberg L. Similarities and differences in the neural correlates of episodic memory retrieval and working memory. Neuroimage 2002, 16:317-330.
10. Callicott J.H., Mattay V.S., Bertolino A., Finn K., Coppola R., Frank J.A., Goldberg T.E., Weinberger D.R. Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cereb. Cortex 1999, 9:20-26.
11. Callicott J.H., Mattay V.S., Verchinski B.A., Marenco S., Egan M.F., Weinberger D.R. Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. Am. J. Psychiatry 2003, 160:2209-2215.
12. Cannon T.D., Zorrilla L.E., Shtasel D., Gur R.E., Gur R.C., Marco E.J., Moberg P., Price R.A. Neuropsychological functioning in siblings discordant for schizophrenia and healthy volunteers. Arch. Gen. Psychiatry 1994, 51:651-661.
13. Chalfonte B.L., Johnson M.K. Feature memory and binding in young and older adults. Mem. Cogn. 1996, 24:403-416.
14. Cohen N.J., Eichenbaum H. The theory that wouldn't die: a critical look at the spatial mapping theory of hippocampal function. Hippocampus 1991, 1:265-268.
15. Dalla Barba G., Parlato V., Jobert A., Samson Y., Pappata S. Cortical networks implicated in semantic and episodic memory: common or unique?. Cortex 1998, 34:547-561.
16. Daselaar S.M., Rombouts S.A., Veltman D.J., Raaijmakers J.G., Lazeron R.H., Jonker C. Parahippocampal activation during successful recognition of words: a self-paced event-related fMRI study. Neuroimage 2001, 13:1113-1120.
17. Davachi L., Wagner A.D. Hippocampal contributions to episodic encoding: insights from relational and item-based learning. J. Neurophysiol. 2002, 88:982-990.
18. Elvevag B., Goldberg T.E. Cognitive impairment in schizophrenia is the core of the disorder. Crit. Rev. Neurobiol. 2000, 14:1-21.
19. First M.B. The Structured Clinical Interview for DSM-IV for Axis I Disorders: Clinical Version, Administration Booklet 1997, American Psychiatric Press, Washington, DC.
20. Gold J.M., Randolph C., Carpenter C.J., Goldberg T.E., Weinberger D.R. Forms of memory failure in schizophrenia. J. Abnorm. Psychol. 1992, 101:487-494.
21. Goldberg T.E., Ragland J.D., Torrey E.F., Gold J.M., Bigelow L.B., Weinberger D.R. Neuropsychological assessment of monozygotic twins discordant for schizophrenia. Arch. Gen. Psychiatry 1990, 47:1066-1072.
22. Goldberg T.E., Straub R.E., Callicott J.H., Hariri A., Mattay V.S., Bigelow L., Coppola R., Egan M.F., Weinberger D.R. The G72/G30 gene complex and cognitive abnormalities in schizophrenia. Neuropsychopharmacology 2006, 31:2022-2032.
23. Goldstein G. Neuropsychological heterogeneity in schizophrenia: a consideration of abstraction and problem-solving abilities. Arch. Clin. Neuropsychol. 1990, 5:251-264.
24. Gottesman I.I., Gould T.D. The endophenotype concept in psychiatry: etymology and strategic intentions. Am. J. Psychiatry 2003, 160:636-645.
25. Gottesman I.I., Shields J. Contributions of twin studies to perspectives on schizophrenia. Prog. Exp. Pers. Res. 1966, 3:1-84.
26. Green M.F. What are the functional consequences of neurocognitive deficits in schizophrenia?. Am. J. Psychiatry 1996, 153:321-330.
27. Hariri A.R., Goldberg T.E., Mattay V.S., Kolachana B.S., Callicott J.H., Egan M.F., Weinberger D.R. Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J. Neurosci. 2003, 23:6690-6694.
28. Heckers S. Neuroimaging studies of the hippocampus in schizophrenia. Hippocampus 2001, 11:520-528.
29. Heckers S., Rauch S.L., Goff D., Savage C.R., Schacter D.L., Fischman A.J., Alpert N.M. Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nat. Neurosci. 1998, 1:318-323.
30. Henson R.N., Rugg M.D., Shallice T., Josephs O., Dolan R.J. Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. J. Neurosci. 1999, 19:3962-3972.
31. Henson R.N., Shallice T., Dolan R.J. Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. Brain 1999, 122(Pt 7):1367-1381.
32. Henson R.N., Rugg M.D., Shallice T., Dolan R.J. Confidence in recognition memory for words: dissociating right prefrontal roles in episodic retrieval. J. Cogn. Neurosci. 2000, 12:913-923.
33. Henson R.N., Hornberger M., Rugg M.D. Further dissociating the processes involved in recognition memory: an FMRI study. J. Cogn. Neurosci. 2005, 17:1058-1073.
34. Herrmann C.S., Munk M.H., Engel A.K. Cognitive functions of gamma-band activity: memory match and utilization. Trends Cogn. Sci. 2004, 8:347-355.
35. Hofer A., Weiss E.M., Golaszewski S.M., Siedentopf C.M., Brinkhoff C., Kremser C., Felber S., Fleischhacker W.W. Neural correlates of episodic encoding and recognition of words in unmedicated patients during an acute episode of schizophrenia: a functional MRI study. Am. J. Psychiatry 2003, 160:1802-1808.
36. Hollingshead A.B. Four-factor Index of Social Status 1975, Yale University, New Haven, CT.
37. Holthausen E.A., Wiersma D., Sitskoorn M.M., Hijman R., Dingemans P.M., Schene A.H., van den Bosch R.J. Schizophrenic patients without neuropsychological deficits: subgroup, disease severity or cognitive compensation?. Psychiatry Res. 2002, 112:1-11.
38. Hong L.E., Summerfelt A., McMahon R., Adami H., Francis G., Elliott A., Buchanan R.W., Thaker G.K. Evoked gamma band synchronization and the liability for schizophrenia. Schizophr. Res. 2004, 70:293-302.
39. Jessen F., Scheef L., Germeshausen L., Tawo Y., Kockler M., Kuhn K.U., Maier W., Schild H.H., Heun R. Reduced hippocampal activation during encoding and recognition of words in schizophrenia patients. Am. J. Psychiatry 2003, 160:1305-1312.
40. Joyce E.M., Roiser J.P. Cognitive heterogeneity in schizophrenia. Curr. Opin. Psychiatry 2007, 20:268-272.
41. Keefe R.S., Silverman J.M., Roitman S.E., Harvey P.D., Duncan M.A., Alroy D., Siever L.J., Davis K.L., Mohs R.C. Performance of nonpsychotic relatives of schizophrenic patients on cognitive tests. Psychiatry Res. 1994, 53:1-12.
42. Kim H. Dissociating the roles of the default-mode, dorsal, and ventral networks in episodic memory retrieval. Neuroimage 2010, 50:1648-1657.
43. Konishi S., Wheeler M.E., Donaldson D.I., Buckner R.L. Neural correlates of episodic retrieval success. Neuroimage 2000, 12:276-286.
44. Lang P., Ohman D.V. The international affective picture system [photographic slides]. Technical Report 1988, The Center for Research in Psychophysiology, University of Florida, Gainsville, FL.
45. Lefebvre A.A., Cellard C., Tremblay S., Achim A., Rouleau N., Maziade M., Roy M.A. Familiarity and recollection processes in patients with recent-onset schizophrenia and their unaffected parents. Psychiatry Res. 2010, 175:15-21.
46. Maguire E.A., Henson R.N., Mummery C.J., Frith C.D. Activity in prefrontal cortex, not hippocampus, varies parametrically with the increasing remoteness of memories. Neuroreport 2001, 12:441-444.
47. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
48. Manoach D.S. Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophr. Res. 2003, 60:285-298.
49. Manoach D.S., Press D.Z., Thangaraj V., Searl M.M., Goff D.C., Halpern E., Saper C.B., Warach S. Schizophrenic subjects activate dorsolateral prefrontal cortex during a working memory task, as measured by fMRI. Biol. Psychiatry 1999, 45:1128-1137.
50. Manoach D.S., Gollub R.L., Benson E.S., Searl M.M., Goff D.C., Halpern E., Saper C.B., Rauch S.L. Schizophrenic subjects show aberrant fMRI activation of dorsolateral prefrontal cortex and basal ganglia during working memory performance. Biol. Psychiatry 2000, 48:99-109.
51. Maziade M., Rouleau N., Merette C., Cellard C., Battaglia M., Marino C., Jomphe V., Gilbert E., Achim A., Bouchard R.H., Paccalet T., Paradis M.E., Roy M.A. Verbal and visual memory impairments among young offspring and healthy adult relatives of patients with schizophrenia and bipolar disorder: selective generational patterns indicate different developmental trajectories. Schizophr. Bull. 2011, 37:1218-1228.
52. McDermott K.B., Ojemann J.G., Petersen S.E., Ollinger J.M., Snyder A.Z., Akbudak E., Conturo T.E., Raichle M.E. Direct comparison of episodic encoding and retrieval of words: an event-related fMRI study. Memory 1999, 7:661-678.
53. Meltzer H.Y., McGurk S.R. The effects of clozapine, risperidone, and olanzapine on cognitive function in schizophrenia. Schizophr. Bull. 1999, 25:233-255.
54. Palmer B.W., Heaton R.K., Paulsen J.S., Kuck J., Braff D., Harris M.J., Zisook S., Jeste D.V. Is it possible to be schizophrenic yet neuropsychologically normal?. Neuropsychology 1997, 11:437-446.
55. Pandya D.N., Yeterian E.H. Comparison of prefrontal architecture and connections. Philos. Trans. R Soc. Lond. B Biol. Sci. 1996, 351:1423-1432.
56. Paulsen J.S., Heaton R.K., Sadek J.R., Perry W., Delis D.C., Braff D., Kuck J., Zisook S., Jeste D.V. The nature of learning and memory impairments in schizophrenia. J. Int. Neuropsychol. Soc. 1995, 1:88-99.
57. Peterson L.R., Peterson M.J. Short-term retention of individual verbal items. J. Exp. Psychol. 1959, 58:193-198.
58. Ragland J.D., Laird A.R., Ranganath C., Blumenfeld R.S., Gonzales S.M., Glahn D.C. Prefrontal activation deficits during episodic memory in schizophrenia. Am. J. Psychiatry 2009, 166:863-874.
59. Reichenberg A., Harvey P.D. Neuropsychological impairments in schizophrenia: integration of performance-based and brain imaging findings. Psychol. Bull. 2007, 133:833-858.
60. Reichenberg A., Rabinowitz J., Weiser M., Mark M., Kaplan Z., Davidson M. Premorbid functioning in a national population of male twins discordant for psychoses. Am. J. Psychiatry 2000, 157:1514-1516.
61. Rugg M.D., Henson R.N., Robb W.G. Neural correlates of retrieval processing in the prefrontal cortex during recognition and exclusion tasks. Neuropsychologia 2003, 41:40-52.
62. Schlösser R., Gesierich T., Kaufmann B., Vucurevic G., Hunsche S., Gawehn J., Stoeter P. Altered effective connectivity during working memory performance in schizophrenia: a study with fMRI and structural equation modeling. Neuroimage 2003, 19:751-763.
63. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 1957, 20:11-21.
64. Seidman L.J., Lanca M., Kremen W.S., Faraone S.V., Tsuang M.T. Organizational and visual memory deficits in schizophrenia and bipolar psychoses using the Rey-Osterrieth complex figure: effects of duration of illness. J. Clin. Exp. Neuropsychol. 2003, 25:949-964.
65. Shallice T., Burgess P. The domain of supervisory processes and temporal organization of behaviour. Philos. Trans. R Soc. Lond. B Biol. Sci. 1996, 351:1405-1411. (discussion 1411-1402).
66. Sheth S.A., Nemoto M., Guiou M., Walker M., Pouratian N., Toga A.W. Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamic responses. Neuron 2004, 42:347-355.
67. Skelley S.L., Goldberg T.E., Egan M.F., Weinberger D.R., Gold J.M. Verbal and visual memory: characterizing the clinical and intermediate phenotype in schizophrenia. Schizophr. Res. 2008, 105:78-85.
68. Snitz B.E., MacDonald A.W., Carter C.S. Cognitive deficits in unaffected first-degree relatives of schizophrenia patients: a meta-analytic review of putative endophenotypes. Schizophr. Bull. 2006, 32:179-194.
69. Uhlhaas P.J., Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 2010, 11:100-113.
70. Vandenberghe R., Price C., Wise R., Josephs O., Frackowiak R.S. Functional anatomy of a common semantic system for words and pictures. Nature 1996, 383:254-256.
71. Ward B.D. Simultaneous Inference for fMRI Data 2000, Author, Milwaukee, WI.
72. Weinberger D.R., Berman K.F., Suddath R., Torrey E.F. Evidence of dysfunction of a prefrontal-limbic network in schizophrenia: a magnetic resonance imaging and regional cerebral blood flow study of discordant monozygotic twins. Am. J. Psychiatry 1992, 149:890-897.
73. Weiss A.P., Heckers S. Neuroimaging of declarative memory in schizophrenia. Scand. J. Psychol. 2001, 42:239-250.
74. Weiss A.P., Schacter D.L., Goff D.C., Rauch S.L., Alpert N.M., Fischman A.J., Heckers S. Impaired hippocampal recruitment during normal modulation of memory performance in schizophrenia. Biol. Psychiatry 2003, 53:48-55.
75. Yonelinas A.P., Levy B.J. Dissociating familiarity from recollection in human recognition memory: different rates of forgetting over short retention intervals. Psychon. Bull. Rev. 2002, 9:575-582.