Testing long-term memory in animal models of schizophrenia: Suggestions from CNTRICS

Neuroscience and Biobehavioral Reviews

Volumn 37, Issue 9, 2013, Pages 2141-2148

  Bussey, Timothy J ^a   Barch, Deanna M ^b   Baxter, Mark G ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b WASHINGTON UNIVERSITY   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Episodic memory; Hippocampus; Mouse; Neuropsychiatric disease; Object recognition; Paired associate learning; Prefrontal cortex; Rat; Relational memory; Rodent; Touchscreen

Indexed keywords

DONEPEZIL;

ASSOCIATIVE MEMORY; BRAIN DYSFUNCTION; COGNITIVE DEFECT; DECLARATIVE MEMORY; DISEASE SEVERITY; EPISODIC MEMORY; HIPPOCAMPUS; HUMAN; LEARNING; LEARNING DISORDER; LONG TERM MEMORY; MEDICAL EDUCATION; MEDICAL RESEARCH; MEMORY DISORDER; MENTAL PERFORMANCE; MENTAL TASK; NONHUMAN; PRIMATE; PRIORITY JOURNAL; RECALL; RECOGNITION; REVIEW; RODENT; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; SYMPTOM; UNITED STATES; WORKING MEMORY;

EPISODIC MEMORY; HIPPOCAMPUS; MOUSE; NEUROPSYCHIATRIC DISEASE; OBJECT RECOGNITION; PAIRED-ASSOCIATE LEARNING; PREFRONTAL CORTEX; RAT; RELATIONAL MEMORY; RODENT; TOUCHSCREEN;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MEMORY DISORDERS; MEMORY, LONG-TERM; SCHIZOPHRENIA;

EID: 84888848692     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2013.06.005     Document Type: Review

References (114)

1. Achim A.M., Lepage M. Is associative recognition more impaired than item recognition memory in Schizophrenia? A meta-analysis. Brain and Cognition 2003, 53:121-124.
2. Aggleton J.P., Brown M.W. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. The Behavioral and Brain Sciences 1999, 22:425-444. (discussion 444-489).
3. Aggleton J.P., McMackin D., Carpenter K., Hornak J., Kapur N., Halpin S., Wiles C.M., Kamel H., Brennan P., Carton S., Gaffan D. Differential cognitive effects of colloid cysts in the third ventricle that spare or compromise the fornix. Brain 2000, 123(Pt 4):800-815.
4. Aubin G., Stip E., Gélinas I., Rainville C., Chapparo C. Daily functioning and information-processing skills among persons with schizophrenia. Psychiatric Services 2009, 60:817-822.
5. Barch D.M. The cognitive neuroscience of schizophrenia. Annual Review of Clinical Psychology 2005, 1:321-353.
6. Barker G.R.I., Warburton E.C. When is the hippocampus involved in recognition memory?. Journal of Neuroscience 2011, 31:10721-10731.
7. Barnett J.H., Sahakian B.J., Werners U., Hill K.E., Brazil R., Gallagher O., Bullmore E.T., Jones P.B. Visuospatial learning and executive function are independently impaired in first-episode psychosis. Psychological Medicine 2005, 35:1031-1041.
8. Bartko S.J., Cowell R.A., Winters B.D., Bussey T.J., Saksida L.M. Heightened susceptibility to interference in an animal model of amnesia: impairment in encoding, storage, retrieval - or all three?. Neuropsychologia 2010, 48:2987-2997.
9. Bartko S.J., Romberg C., White B., Wess J., Bussey T.J., Saksida L.M. Intact attentional processing but abnormal responding in M1 muscarinic receptor-deficient mice using an automated touchscreen method. Neuropharmacology 2011, 61:1366-1378.
10. Bartko S.J., Vendrell I., Saksida L.M., Bussey T.J. A computer-automated touchscreen paired-associates learning (PAL) task for mice: impairments following administration of scopolamine or dicyclomine and improvements following donepezil. Psychopharmacology 2011, 214:537-548.
11. Bartko S.J., Winters B.D., Cowell R.A., Saksida L.M., Bussey T.J. Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations. The Journal of Neuroscience 2007, 27:2548-2559.
12. Bartko S.J., Winters B.D., Cowell R.A., Saksida L.M., Bussey T.J. Perirhinal cortex resolves feature ambiguity in configural object recognition and perceptual oddity tasks. Learning & Memory 2007, 14:821-832.
13. Bartók E., Berecz R., Glaub T., Degrell I. Cognitive functions in prepsychotic patients. Progress in Neuro-Psychopharmacology & Biological Psychiatry 2005, 29:621-625.
14. Baxter M.G., Browning P.G.F., Mitchell A.S. Perseverative interference with object-in-place scene learning in rhesus monkeys with bilateral ablation of ventrolateral prefrontal cortex. Learning & Memory 2008, 15:126-132.
15. Baxter M.G., Gaffan D., Kyriazis D.A., Mitchell A.S. Orbital prefrontal cortex is required for object-in-place scene memory but not performance of a strategy implementation task. The Journal of Neuroscience 2007, 27:11327-11333.
16. Blumenfeld R.S., Parks C.M., Yonelinas A.P., Ranganath C. Putting the pieces together: the role of dorsolateral prefrontal cortex in relational memory encoding. Journal of Cognitive Neuroscience 2011, 23:257-265.
17. Bonner-Jackson A., Haut K., Csernansky J.G., Barch D.M. The influence of encoding strategy on episodic memory and cortical activity in schizophrenia. Biological Psychiatry 2005, 58:47-55.
18. Brébion G., Smith M.J., Gorman J.M., Amador X. Discrimination accuracy and decision biases in different types of reality monitoring in schizophrenia. The Journal of Nervous and Mental Disease 1997, 185:247-253.
19. Browning P.G.F., Easton A., Buckley M.J., Gaffan D. The role of prefrontal cortex in object-in-place learning in monkeys. European Journal of Neuroscience 2005, 22:3281-3291.
20. Bryson J.J., Leong J.C.S. Primate errors in transitive inference: a two-tier learning model. Animal Cognition 2007, 10:1-15.
21. Burke S.N., Wallace J.L., Hartzell A.L., Nematollahi S., Plange K., Barnes C.A. Age-associated deficits in pattern separation functions of the perirhinal cortex: a cross-species consensus. Behavioral Neuroscience 2011, 125:836-847.
22. Chiba A.A., Kesner R.P., Gibson C.J. Memory for temporal order of new and familiar spatial location sequences: role of the medial prefrontal cortex. Learning & Memory 1997, 4:311-317.
23. Chiba A.A., Kesner R.P., Reynolds A.M. Memory for spatial location as a function of temporal lag in rats: role of hippocampus and medial prefrontal cortex. Behavioral and Neural Biology 1994, 61:123-131.
24. Chouinard S., Stip E., Poulin J., Melun J.-P., Godbout R., Guillem F., Cohen H. Rivastigmine treatment as an add-on to antipsychotics in patients with schizophrenia and cognitive deficits. Current Medical Research and Opinion 2007, 23:575-583.
25. Clayton N.S., Bussey T.J., Dickinson A. Can animals recall the past and plan for the future?. Nature Reviews: Neuroscience 2003, 4:685-691.
26. Clayton N.S., Dickinson A. Episodic-like memory during cache recovery by scrub jays. Nature 1998, 395:272-274.
27. Clayton N.S., Griffiths D.P., Emery N.J., Dickinson A. Elements of episodic-like memory in animals. Philosophical Transactions of the Royal Society B: Biological Sciences 2001, 356:1483-1491.
28. Clelland C.D., Choi M., Romberg C., Clemenson G.D., Fragniere A., Tyers P., Jessberger S., Saksida L.M., Barker R.A., Gage F.H., Bussey T.J. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009, 325:210-213.
29. Croxson P.L., Browning P.G.F., Gaffan D., Baxter M.G. Acetylcholine facilitates recovery of episodic memory after brain damage. The Journal of Neuroscience 2012, 32:13787-13795.
30. Danion J.-M., Huron C., Vidailhet P., Berna F. Functional mechanisms of episodic memory impairment in schizophrenia. Canadian Journal of Psychiatry 2007, 52:693-701.
31. Day M., Langston R., Morris R.G.M. Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 2003, 424:205-209.
32. Dean B., Bymaster F.P., Scarr E. Muscarinic receptors in schizophrenia. Current Molecular Medicine 2003, 3:419-426.
33. Dere E., Huston J.P., De Souza Silva M.A. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neuroscience and Biobehavioral Reviews 2007, 31:673-704.
34. Devito L.M., Eichenbaum H. Distinct contributions of the hippocampus and medial prefrontal cortex to the what-where-when components of episodic-like memory in mice. Behavioural Brain Research 2010, 215:318-325.
35. Diaz-Asper C., Malley J., Genderson M., Apud J., Elvevåg B. Context binding in schizophrenia: effects of clinical symptomatology and item content. Psychiatry Research 2008, 159:259-270.
36. Dix S.L., Aggleton J.P. Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behavioural Brain Research 1999, 99:191-200.
37. Donohoe G., Spoletini I., McGlade N., Behan C., Hayden J., O'Donoghue T., Peel R., Haq F., Walker C., O'Callaghan E., Spalletta G., Gill M., Corvin A. Are relational style and neuropsychological performance predictors of social attributions in chronic schizophrenia?. Psychiatry Research 2008, 161:19-27.
38. Dudchenko P.A., Talpos J., Young J., Baxter M.G. Animal models of working memory: a review of tasks that might be used in screening drug treatments for the memory impairments found in schizophrenia. Neuroscience and Biobehavioral Reviews 2013, (in press). 10.1016/j.neubiorev.2012.03.003.
39. Eacott M.J., Easton A., Zinkivskay A. Recollection in an episodic-like memory task in the rat. Learning & Memory 2005, 12:221-223.
40. Eacott M.J., Norman G. Integrated memory for object, place, and context in rats: a possible model of episodic-like memory. The Journal of Neuroscience 2004, 24:1948-1953.
41. Easton A., Fitchett A.E., Eacott M.J., Baxter M.G. Medial septal cholinergic neurons are necessary for context-place memory but not episodic-like memory. Hippocampus 2011, 21:1021-1027.
42. Eichenbaum H., Cohen N.J. From Conditioning to Conscious Recollection 2004, Oxford University Press, USA.
43. Elvevåg B., Egan M.F., Goldberg T.E. Memory for temporal order in patients with schizophrenia. Schizophrenia Research 2000, 46:187-193.
44. Esslinger C., Walter H., Kirsch P., Erk S., Schnell K., Arnold C., Haddad L., Mier D., Opitz von Boberfeld C., Raab K., Witt S.H., Rietschel M., Cichon S., Meyer-Lindenberg A. Neural mechanisms of a genome-wide supported psychosis variant. Science 2009, 324:605.
45. Freedman R., Olincy A., Buchanan R.W., Harris J.G., Gold J.M., Johnson L., Allensworth D., Guzman-Bonilla A., Clement B., Ball M.P., Kutnick J., Pender V., Martin L.F., Stevens K.E., Wagner B.D., Zerbe G.O., Soti F., Kem W.R. Initial phase 2 trial of a nicotinic agonist in schizophrenia. The American Journal of Psychiatry 2008, 165:1040-1047.
46. Gaffan D. Scene-specific memory for objects: a model of episodic memory impairment in monkeys with fornix transection. Journal of Cognitive Neuroscience 1994, 6:305-320.
47. Gaffan D. Against memory systems. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2002, 357:1111-1121.
48. Gaffan D., Parker A. Mediodorsal thalamic function in scene memory in rhesus monkeys. Brain 2000, 123(Pt 4):816-827.
49. Gaffan D., Parker A., Easton A. Dense amnesia in the monkey after transection of fornix, amygdala and anterior temporal stem. Neuropsychologia 2001, 39:51-70.
50. Gaffan E.A., Bannerman D.M., Warburton E.C., Aggleton J.P. Rats' processing of visual scenes: effects of lesions to fornix, anterior thalamus, mamillary nuclei or the retrohippocampal region. Behavioural Brain Research 2001, 121:103-117.
51. Gaffan E.A., Eacott M.J. Spatial memory impairment in rats with fornix transection is not accompanied by a simple encoding deficit for directions of objects in visual space. Behavioral Neuroscience 1997, 111:937-954.
52. Good M.A., Barnes P., Staal V., McGregor A., Honey R.C. Context- but not familiarity-dependent forms of object recognition are impaired following excitotoxic hippocampal lesions in rats. Behavioral Neuroscience 2007, 121:218-223.
53. Griffiths D., Dickinson A., Clayton N. Episodic memory: what can animals remember about their past?. Trends in Cognitive Sciences (Regul. Ed.) 1999, 3:74-80.
54. Hanlon F.M., Houck J.M., Pyeatt C.J., Lundy S.L., Euler M.J., Weisend M.P., Thoma R.J., Bustillo J.R., Miller G.A., Tesche C.D. Bilateral hippocampal dysfunction in schizophrenia. Neuroimage 2011, 58:1158-1168.
55. Hannula D.E., Ranganath C. The eyes have it: hippocampal activity predicts expression of memory in eye movements. Neuron 2009, 63:592-599.
56. Hannula D.E., Ranganath C., Ramsay I.S., Solomon M., Yoon J., Niendam T.A., Carter C.S., Ragland J.D. Use of eye movement monitoring to examine item and relational memory in schizophrenia. Biological Psychiatry 2010, 68:610-616.
57. Heckers S., Zalesak M., Weiss A.P., Ditman T., Titone D. Hippocampal activation during transitive inference in humans. Hippocampus 2004, 14:153-162.
58. Hill S.K., Griffin G.B., Houk J.C., Sweeney J.A. Differential effects of paced and unpaced responding on delayed serial order recall in schizophrenia. Schizophrenia Research 2011, 131:192-197.
59. Hoge J., Kesner R.P. Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects. Neurobiology of Learning and Memory 2007, 88:225-231.
60. Horner A.E., Romberg C., Bussey T.J., Saksida L.M. Acquisition of a mouse touchscreen object-location Paired Associate Learning (PAL) task does not require the dorsal hippocampus. Presented at the British Neuroscience Association Annual Meeting 2011.
61. Hunsaker M.R., Fieldsted P.M., Rosenberg J.S., Kesner R.P. Dissociating the roles of dorsal and ventral CA1 for the temporal processing of spatial locations, visual objects, and odors. Behavioral Neuroscience 2008, 122:643-650.
62. International Schizophrenia Consortium Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 2008, 455:237-241.
63. Janowsky J.S., Shimamura A.P., Kritchevsky M., Squire L.R. Cognitive impairment following frontal lobe damage and its relevance to human amnesia. Behavioral Neuroscience 1989, 103:548-560.
64. Janowsky J.S., Shimamura A.P., Squire L.R. Source memory impairment in patients with frontal lobe lesions. Neuropsychologia 1989, 27:1043-1056.
65. Johnson M.K., Hashtroudi S., Lindsay D.S. Source monitoring. Psychological Bulletin 1993, 114:3-28.
66. Keefe R.S., Arnold M.C., Bayen U.J., Harvey P.D. Source monitoring deficits in patients with schizophrenia; a multinomial modelling analysis. Psychological Medicine 1999, 29:903-914.
67. Kesner R.P., Hunsaker M.R. The temporal attributes of episodic memory. Behavioural Brain Research 2010, 215:299-309.
68. Kim J.J., Clark R.E., Thompson R.F. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behavioral Neuroscience 1995, 109:195-203.
69. Langston R.F., Wood E.R. Associative recognition and the hippocampus: differential effects of hippocampal lesions on object-place, object-context and object-place-context memory. Hippocampus 2010, 20:1139-1153.
70. Libby L.A., Yonelinas A.P., Ranganath C., Ragland J.D. Recollection and familiarity in schizophrenia: a quantitative review. Biological Psychiatry 2012, 10.1016/j.biopsych.2012.10.027.
71. Lisman J.E., Coyle J.T., Green R.W., Javitt D.C., Benes F.M., Heckers S., Grace A.A. Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends in Neurosciences 2008, 31:234-242.
72. Lyon L., Saksida L.M., Bussey T.J. Spontaneous object recognition and its relevance to schizophrenia: a review of findings from pharmacological, genetic, lesion and developmental rodent models. Psychopharmacology 2012, 220:647-672.
73. Manns J.R., Stark C.E., Squire L.R. The visual paired-comparison task as a measure of declarative memory. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:12375-12379.
74. Marenco S., Weinberger D.R., Schreurs B.G. Single-cue delay and trace classical conditioning in schizophrenia. Biological Psychiatry 2003, 53:390-402.
75. McGlinchey-Berroth R., Carrillo M.C., Gabrieli J.D., Brawn C.M., Disterhoft J.F. Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behavioral Neuroscience 1997, 111:873-882.
76. Meyer-Lindenberg A.S., Olsen R.K., Kohn P.D., Brown T., Egan M.F., Weinberger D.R., Berman K.F. Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Archives of General Psychiatry 2005, 62:379-386.
77. Mitchell A.S., Baxter M.G., Gaffan D. Dissociable performance on scene learning and strategy implementation after lesions to magnocellular mediodorsal thalamic nucleus. The Journal of Neuroscience 2007, 27:11888-11895.
78. Murray E.A., Baxter M.G., Gaffan D. Monkeys with rhinal cortex damage or neurotoxic hippocampal lesions are impaired on spatial scene learning and object reversals. Behavioral Neuroscience 1998, 112:1291-1303.
79. Nemanic S., Alvarado M.C., Bachevalier J. The hippocampal/parahippocampal regions and recognition memory: insights from visual paired comparison versus object-delayed nonmatching in monkeys. The Journal of Neuroscience 2004, 24:2013-2026.
80. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nature Neuroscience 2010, 13:1161-1169.
81. Nilsson M., Hansson S., Carlsson A., Carlsson M.L. Differential effects of the N-methyl-d-aspartate receptor antagonist MK-801 on different stages of object recognition memory in mice. Neuroscience 2007, 149:123-130.
82. Nithianantharajah J., Komiyama N.H., McKechanie A., Johnstone M., Blackwood D.H., St Clair D., Emes R.D., van de Lagemaat L.N., Saksida L.M., Bussey T.J., Grant S.G.N. Synaptic scaffold evolution generated components of vertebrate cognitive complexity. Nature Neuroscience 2013, 16:16-24.
83. Norman G., Eacott M.J. Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions. Behavioural Brain Research 2004, 148:79-91.
84. Pastalkova E., Serrano P., Pinkhasova D., Wallace E., Fenton A.A., Sacktor T.C. Storage of spatial information by the maintenance mechanism of LTP. Science 2006, 313:1141-1144.
85. Prouteau A., Verdoux H., Briand C., Lesage A., Lalonde P., Nicole L., Reinharz D., Stip E. Self-assessed cognitive dysfunction and objective performance in outpatients with schizophrenia participating in a rehabilitation program. Schizophrenia Research 2004, 69:85-91.
86. Prouteau A., Verdoux H., Briand C., Lesage A., Lalonde P., Nicole L., Reinharz D., Stip E. Cognitive predictors of psychosocial functioning outcome in schizophrenia: a follow-up study of subjects participating in a rehabilitation program. Schizophrenia Research 2005, 77:343-353.
87. Ragland J.D., Cools R., Frank M., Pizzagalli D.A., Preston A., Ranganath C., Wagner A.D. CNTRICS final task selection: long-term memory. Schizophrenia Bulletin 2009, 35:197-212.
88. 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. The American Journal of Psychiatry 2009, 166:863-874.
89. Ragland J.D., Ranganath C., Barch D.M., Gold J.M., Haley B., MacDonald A.W., Silverstein S.M., Strauss M.E., Yonelinas A.P., Carter C.S. Relational and Item-Specific Encoding (RISE): task development and psychometric characteristics. Schizophrenia Bulletin 2012, 38:114-124.
90. Ranganath C., Minzenberg M.J., Ragland J.D. The cognitive neuroscience of memory function and dysfunction in schizophrenia. Biological Psychiatry 2008, 64:18-25.
91. Rapp P.R., Kansky M.T., Eichenbaum H. Learning and memory for hierarchical relationships in the monkey: effects of aging. Behavioral Neuroscience 1996, 110:887-897.
92. Ritsner M.S., Blumenkrantz H. Predicting domain-specific insight of schizophrenia patients from symptomatology, multiple neurocognitive functions, and personality related traits. Psychiatry Research 2007, 149:59-69.
93. Romberg C., Horner A.E., Bussey T.J., Saksida L.M. A touch screen-automated cognitive test battery reveals impaired attention, memory abnormalities, and increased response inhibition in the TgCRND8 mouse model of Alzheimer's disease. Neurobiology of Aging 2012, 34:731-744.
94. Shimamura A.P., Janowsky J.S., Squire L.R. Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients. Neuropsychologia 1990, 28:803-813.
95. Smith C., Squire L.R. Declarative memory, awareness, and transitive inference. The Journal of Neuroscience 2005, 25:10138-10146.
96. Solomon P.R., Vander Schaaf E.R., Thompson R.F., Weisz D.J. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behavioral Neuroscience 1986, 100:729-744.
97. Spaniol J., Davidson P.S.R., Kim A.S.N., Han H., Moscovitch M., Grady C.L. Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 2009, 47:1765-1779.
98. Squire L.R. Memory and Brain 1987, Oxford University Press, USA.
99. Stip E., Sepehry A.A., Prouteau A., Briand C., Nicole L., Lalonde P., Lesage A. Cognitive discernible factors between schizophrenia and schizoaffective disorder. Brain and Cognition 2005, 59:292-295.
100. Talpos J.C., Winters B.D., Dias R., Saksida L.M., Bussey T.J. A novel touchscreen-automated paired-associate learning (PAL) task sensitive to pharmacological manipulation of the hippocampus: a translational rodent model of cognitive impairments in neurodegenerative disease. Psychopharmacology 2009, 205:157-168.
101. Titone D., Ditman T., Holzman P.S., Eichenbaum H., Levy D.L. Transitive inference in schizophrenia: impairments in relational memory organization. Schizophrenia Research 2004, 68:235-247.
102. van Erp T.G.M., Lesh T.A., Knowlton B.J., Bearden C.E., Hardt M., Karlsgodt K.H., Shirinyan D., Rao V., Green M.F., Subotnik K.L., Nuechterlein K., Cannon T.D. Remember and know judgments during recognition in chronic schizophrenia. Schizophrenia Research 2008, 100:181-190.
103. Vinogradov S., Willis-Shore J., Poole J.H., Marten E., Ober B.A., Shenaut G.K. Clinical and neurocognitive aspects of source monitoring errors in schizophrenia. The American Journal of Psychiatry 1997, 154:1530-1537.
104. Walsh T., McClellan J.M., McCarthy S.E., Addington A.M., Pierce S.B., Cooper G.M., Nord A.S., Kusenda M., Malhotra D., Bhandari A., Stray S.M., Rippey C.F., Roccanova P., Makarov V., Lakshmi B., Findling R.L., Sikich L., Stromberg T., Merriman B., Gogtay N., Butler P., Eckstrand K., Noory L., Gochman P., Long R., Chen Z., Davis S., Baker C., Eichler E.E., Meltzer P.S., Nelson S.F., Singleton A.B., Lee M.K., Rapoport J.L., King M.-C., Sebat J. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 2008, 320:539-543.
105. Waters F. Context memory and binding in schizophrenia. Schizophrenia Research 2004, 68:119-125.
106. Weiss A.P., Zalesak M., DeWitt I., Goff D., Kunkel L., Heckers S. Impaired hippocampal function during the detection of novel words in schizophrenia. Biological Psychiatry 2004, 55:668-675.
107. Wilson C.R.E., Baxter M.G., Easton A., Gaffan D. Addition of fornix transection to frontal-temporal disconnection increases the impairment in object-in-place memory in macaque monkeys. The European Journal of Neuroscience 2008, 27:1814-1822.
108. Wilson C.R.E., Gaffan D., Browning P.G.F., Baxter M.G. Functional localization within the prefrontal cortex: missing the forest for the trees?. Trends in Neurosciences 2010, 33:533-540.
109. Winters B.D., Bussey T.J. Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. The Journal of Neuroscience 2005, 25:4243-4251.
110. Winters B.D., Forwood S.E., Cowell R.A., Saksida L.M., Bussey T.J. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. The Journal of Neuroscience 2004, 24:5901-5908.
111. Winters B.D., Saksida L.M., Bussey T.J. Paradoxical facilitation of object recognition memory after infusion of scopolamine into perirhinal cortex: implications for cholinergic system function. The Journal of Neuroscience 2006, 26:9520-9529.
112. Wood S.J., Proffitt T., Mahony K., Smith D.J., Buchanan J.A., Brewer W., Stuart G.W., Velakoulis D., McGorry P.D., Pantelis C. Visuospatial memory and learning in first-episode schizophreniform psychosis and established schizophrenia: a functional correlate of hippocampal pathology?. Psychological Medicine 2002, 32:429-438.
113. Young J.W., Powell S.B., Risbrough V., Marston H.M., Geyer M.A. Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacology & Therapeutics 2009, 122:150-202.
114. Young J.W., Jentsch J.D., Bussey T.J., Wallace T.L., Hutchenson D.M. Consideration of species differences in developing novel molecules as cognitive enhancers. Neuroscience and Biobehavioral Reviews 2013, (in press). 10.1016/j.neubiorev.2012.10.002.