Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T04:25:23.844Z Has data issue: false hasContentIssue false
  • English
  • Français

Evidence that hippocampal–parahippocampal dysfunction is related to genetic risk for schizophrenia

Published online by Cambridge University Press:  31 October 2012

A. Di Giorgio ,
B. Gelao ,
G. Caforio ,
R. Romano ,
I. Andriola ,
E. D'Ambrosio ,
A. Papazacharias ,
F. Elifani ,
L. Lo Bianco  and
P. Taurisano
...Show all authors
A. Di Giorgio
Affiliation:
IRCCS ‘Casa Sollievo della Sofferenza’, San Giovanni Rotondo, Foggia, Italy
B. Gelao
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
G. Caforio
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
R. Romano
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
I. Andriola
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
E. D'Ambrosio
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
A. Papazacharias
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
F. Elifani
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
L. Lo Bianco
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy Psychiatric Unit, Department of Mental Health, United Hospitals of Ancona, Polytechnic University of Marche, Italy
P. Taurisano
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
L. Fazio
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
T. Popolizio
Affiliation:
IRCCS ‘Casa Sollievo della Sofferenza’, San Giovanni Rotondo, Foggia, Italy
G. Blasi
Affiliation:
Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
A. Bertolino*
Affiliation:
IRCCS ‘Casa Sollievo della Sofferenza’, San Giovanni Rotondo, Foggia, Italy Psychiatric Neuroscience Group, Department of Neuroscience and Sense Organs, University of Bari ‘Aldo Moro’, Bari, Italy
*
*Address for correspondence: A. Bertolino, M.D., Ph.D., Dipartimento di Neuroscienze ed Organi di Senso, Università degli Studi di Bari ‘Aldo Moro’, Piazza Giulio Cesare, 11, 70124, Bari, Italy. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Abnormalities in hippocampal–parahippocampal (H-PH) function are prominent features of schizophrenia and have been associated with deficits in episodic memory. However, it remains unclear whether these abnormalities represent a phenotype related to genetic risk for schizophrenia or whether they are related to disease state.

Method

We investigated H-PH-mediated behavior and physiology, using blood oxygenation level-dependent functional magnetic resonance imaging (BOLD fMRI), during episodic memory in a sample of patients with schizophrenia, clinically unaffected siblings and healthy subjects.

Results

Patients with schizophrenia and unaffected siblings displayed abnormalities in episodic memory performance. During an fMRI memory encoding task, both patients and siblings demonstrated a similar pattern of reduced H-PH engagement compared with healthy subjects.

Conclusions

Our findings suggest that the pathophysiological mechanism underlying the inability of patients with schizophrenia to properly engage the H-PH during episodic memory is related to genetic risk for the disorder. Therefore, H-PH dysfunction can be assumed as a schizophrenia susceptibility-related phenotype.

Keywords

Genetic riskhippocampusmemoryschizophreniasiblings
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 8 , August 2013 , pp. 1661 - 1671
Copyright
Copyright © Cambridge University Press 2012 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Achim, AM, Bertrand, MC, Sutton, H, Montoya, A, Czechowska, Y, Malla, AK, Joober, R, Pruessner, JC, Lepage, M (2007). Selective abnormal modulation of hippocampal activity during memory formation in first-episode psychosis. Archives of General Psychiatry 64, 999–1014.CrossRefGoogle ScholarPubMed
Achim, AM, Lepage, M (2005). Episodic memory-related activation in schizophrenia: meta-analysis. British Journal of Psychiatry 187, 500–509.CrossRefGoogle ScholarPubMed
Aleman, A, Hijman, R, de Haan, EH, Kahn, RS (1999). Memory impairment in schizophrenia: a meta-analysis. American Journal of Psychiatry 156, 1358–1366.CrossRefGoogle ScholarPubMed
Allen, P, Chaddock, CA, Howes, OD, Egerton, A, Seal, ML, Fusar-Poli, P, Valli, I, Day, F, McGuire, PK (2012). Abnormal relationship between medial temporal lobe and subcortical dopamine function in people with an ultra high risk for psychosis. Schizophrenia Bulletin 38, 1040–1049.CrossRefGoogle ScholarPubMed
Allen, P, Seal, ML, Valli, I, Fusar-Poli, P, Perlini, C, Day, F, Wood, SJ, Williams, SC, McGuire, PK (2011). Altered prefrontal and hippocampal function during verbal encoding and recognition in people with prodromal symptoms of psychosis. Schizophrenia Bulletin 37, 746–756.CrossRefGoogle ScholarPubMed
Bertolino, A, Di Giorgio, A, Blasi, G, Sambataro, F, Caforio, G, Sinibaldi, L, Latorre, V, Rampino, A, Taurisano, P, Fazio, L, Romano, R, Douzgou, S, Popolizio, T, Kolachana, B, Nardini, M, Weinberger, DR, Dallapiccola, B (2008). Epistasis between dopamine regulating genes identifies a nonlinear response of the human hippocampus during memory tasks. Biological Psychiatry 64, 226–234.CrossRefGoogle ScholarPubMed
Bertolino, A, Rubino, V, Sambataro, F, Blasi, G, Latorre, V, Fazio, L, Caforio, G, Petruzzella, V, Kolachana, B, Hariri, A, Meyer-Lindenberg, A, Nardini, M, Weinberger, DR, Scarabino, T (2006). Prefrontal-hippocampal coupling during memory processing is modulated by COMT Val158Met genotype. Biological Psychiatry 60, 1250–1258.CrossRefGoogle ScholarPubMed
Bigos, KL, Mattay, VS, Callicott, JH, Straub, RE, Vakkalanka, R, Kolachana, B, Hyde, TM, Lipska, BK, Kleinman, JE, Weinberger, DR (2010). Genetic variation in CACNA1C affects brain circuitries related to mental illness. Archives of General Psychiatry 67, 939–945.CrossRefGoogle ScholarPubMed
Bonner-Jackson, A, Csernansky, JG, Barch, DM (2007). Levels-of-processing effects in first-degree relatives of individuals with schizophrenia. Biological Psychiatry 61, 1141–1147.CrossRefGoogle ScholarPubMed
Callicott, JH, Egan, MF, Bertolino, A, Mattay, VS, Langheim, FJ, Frank, JA, Weinberger, DR (1998). Hippocampal N-acetyl aspartate in unaffected siblings of patients with schizophrenia: a possible intermediate neurobiological phenotype. Biological Psychiatry 44, 941–950.CrossRefGoogle ScholarPubMed
Callicott, JH, Straub, RE, Pezawas, L, Egan, MF, Mattay, VS, Hariri, AR, Verchinski, BA, Meyer-Lindenberg, A, Balkissoon, R, Kolachana, BS, Goldberg, TE, Weinberger, DR (2005). Variation in DISC1 affects hippocampal structure and function and increases risk for schizophrenia. Proceedings of the National Academy of Sciences USA 102, 8627–8632.CrossRefGoogle ScholarPubMed
Cannon, TD, Zorrilla, LE, Shtasel, D, Gur, RE, Gur, RC, Marco, EJ, Moberg, P, Price, RA (1994). Neuropsychological functioning in siblings discordant for schizophrenia and healthy volunteers. Archives of General Psychiatry 51, 651–661.CrossRefGoogle ScholarPubMed
Danion, JM, Huron, C, Vidailhet, P, Berna, F (2007). Functional mechanisms of episodic memory impairment in schizophrenia. Canadian Journal of Psychiatry 52, 693–701.CrossRefGoogle ScholarPubMed
Di Giorgio, A, Blasi, G, Sambataro, F, Rampino, A, Papazacharias, A, Gambi, F, Romano, R, Caforio, G, Rizzo, M, Latorre, V, Popolizio, T, Kolachana, B, Callicott, JH, Nardini, M, Weinberger, DR, Bertolino, A (2008). Association of the SerCys DISC1 polymorphism with human hippocampal formation gray matter and function during memory encoding. European Journal of Neuroscience 28, 2129–2136.CrossRefGoogle ScholarPubMed
Di Giorgio, A, Caforio, G, Blasi, G, Taurisano, P, Fazio, L, Romano, R, Ursini, G, Gelao, B, Lo Bianco, L, Papazacharias, A, Sinibaldi, L, Popolizio, T, Bellomo, A, Bertolino, A (2011). Catechol-O-methyltransferase Val158Met association with parahippocampal physiology during memory encoding in schizophrenia. Psychological Medicine 41, 1721–1731.CrossRefGoogle ScholarPubMed
Di Giorgio, A, Sambataro, F, Bertolino, A (2009). Functional imaging as a tool to investigate the relationship between genetic variation and response to treatment with antipsychotics. Current Pharmaceutical Design 15, 2560–2572.CrossRefGoogle ScholarPubMed
Egan, MF, Kojima, M, Callicott, JH, Goldberg, TE, Kolachana, BS, Bertolino, A, Zaitsev, E, Gold, B, Goldman, D, Dean, M, Lu, B, Weinberger, DR (2003). The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112, 257–269.CrossRefGoogle ScholarPubMed
Egan, MF, Straub, RE, Goldberg, TE, Yakub, I, Callicott, JH, Hariri, AR, Mattay, VS, Bertolino, A, Hyde, TM, Shannon-Weickert, C, Akil, M, Crook, J, Vakkalanka, RK, Balkissoon, R, Gibbs, RA, Kleinman, JE, Weinberger, DR (2004). Variation in GRM3 affects cognition, prefrontal glutamate, and risk for schizophrenia. Proceedings of the National Academy of Sciences USA 101, 12604–12609.CrossRefGoogle ScholarPubMed
Faraone, SV, Seidman, LJ, Kremen, WS, Pepple, JR, Lyons, MJ, Tsuang, MT (1995). Neuropsychological functioning among the nonpsychotic relatives of schizophrenic patients: a diagnostic efficiency analysis. Journal of Abnormal Psychology 104, 286–304.CrossRefGoogle ScholarPubMed
Faraone, SV, Seidman, LJ, Kremen, WS, Toomey, R, Pepple, JR, Tsuang, MT (1999). Neuropsychological functioning among the nonpsychotic relatives of schizophrenic patients: a 4-year follow-up study. Journal of Abnormal Psychology 108, 176–181.CrossRefGoogle ScholarPubMed
Faraone, SV, Seidman, LJ, Kremen, WS, Toomey, R, Pepple, JR, Tsuang, MT (2000). Neuropsychologic functioning among the nonpsychotic relatives of schizophrenic patients: the effect of genetic loading. Biological Psychiatry 48, 120–126.CrossRefGoogle Scholar
First, MB, Gibbon, M, Spitzer, RL, Williams, JBW (1996). Guide for the Structured Clinical Interview for DSM-IV Axis I Disorders – Research Version. Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
Freedman, R, Leonard, S, Olincy, A, Kaufmann, CA, Malaspina, D, Cloninger, CR, Svrakic, D, Faraone, SV, Tsuang, MT (2001). Evidence for the multigenic inheritance of schizophrenia. American Journal of Medical Genetics 105, 794–800.CrossRefGoogle ScholarPubMed
Friston, K (2003). Introduction: Experimental design and statistical parametric mapping. In Human Brain Function (ed. Frackowiak, R., Friston, K., Frith, C., Dolan, R., Friston, K., Price, C., Zeki, S., Ashburner, J. and Penny, W.), pp. 1–67. Academic Press: London.Google Scholar
Gold, JM (2004). Cognitive deficits as treatment targets in schizophrenia. Schizophrenia Research 72, 21–28.CrossRefGoogle ScholarPubMed
Goldberg, T, David, A, Gold, J (2011). Neurocognitive impairments in schizophrenia: their character and role in symptom formation. In Schizophrenia, 3rd edn (ed. Weinberger, D. and Harrison, P.), pp. 142–162. Wiley-Blackwell: Chichester, UK.Google ScholarPubMed
Goldberg, TE, Egan, MF, Gscheidle, T, Coppola, R, Weickert, T, Kolachana, BS, Goldman, D, Weinberger, DR (2003). Executive subprocesses in working memory: relationship to catechol-O-methyltransferase Val158Met genotype and schizophrenia. Archives of General Psychiatry 60, 889–896.CrossRefGoogle ScholarPubMed
Goldberg, TE, Straub, RE, Callicott, JH, Hariri, A, Mattay, VS, Bigelow, L, Coppola, R, Egan, MF, Weinberger, DR (2006). The G72/G30 gene complex and cognitive abnormalities in schizophrenia. Neuropsychopharmacology 31, 2022–2032.CrossRefGoogle ScholarPubMed
Green, MF (1996). What are the functional consequences of neurocognitive deficits in schizophrenia? American Journal of Psychiatry 153, 321–330.Google ScholarPubMed
Gur, RE, Calkins, ME, Gur, RC, Horan, WP, Nuechterlein, KH, Seidman, LJ, Stone, WS (2007). The Consortium on the Genetics of Schizophrenia: neurocognitive endophenotypes. Schizophrenia Bulletin 33, 49–68.CrossRefGoogle Scholar
Hariri, AR, Goldberg, TE, Mattay, VS, Kolachana, BS, Callicott, JH, Egan, MF, Weinberger, DR (2003). Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. Journal of Neuroscience 23, 6690–6694.CrossRefGoogle ScholarPubMed
Harrison, P, Lewis, D (2003). Neuropathology of schizophrenia. In Schizophrenia (ed. Hirsch, S. and Weinberger, D.), pp. 310–325. Blackwell Science: Oxford.CrossRefGoogle ScholarPubMed
Honea, R, Crow, TJ, Passingham, D, Mackay, CE (2005). Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. American Journal of Psychiatry 162, 2233–2245.CrossRefGoogle ScholarPubMed
Huffaker, SJ, Chen, J, Nicodemus, KK, Sambataro, F, Yang, F, Mattay, V, Lipska, BK, Hyde, TM, Song, J, Rujescu, D, Giegling, I, Mayilyan, K, Proust, MJ, Soghoyan, A, Caforio, G, Callicott, JH, Bertolino, A, Meyer-Lindenberg, A, Chang, J, Ji, Y, Egan, MF, Goldberg, TE, Kleinman, JE, Lu, B, Weinberger, DR (2009). A primate-specific, brain isoform of KCNH2 affects cortical physiology, cognition, neuronal repolarization and risk of schizophrenia. Nature Medicine 15, 509–518.CrossRefGoogle ScholarPubMed
Karnik-Henry, MS, Wang, L, Barch, DM, Harms, MP, Campanella, C, Csernansky, JG (2012). Medial temporal lobe structure and cognition in individuals with schizophrenia and in their non-psychotic siblings. Schizophrenia Research 138, 128–135.CrossRefGoogle ScholarPubMed
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Keshavan, MS, Dick, E, Mankowski, I, Harenski, K, Montrose, DM, Diwadkar, V, DeBellis, M (2002). Decreased left amygdala and hippocampal volumes in young offspring at risk for schizophrenia. Schizophrenia Research 58, 173–183.CrossRefGoogle ScholarPubMed
Kopald, BE, Mirra, KM, Egan, MF, Weinberger, DR, Goldberg, TE (2012). Magnitude of impact of executive functioning and IQ on episodic memory in schizophrenia. Biological Psychiatry 71, 545–551.CrossRefGoogle ScholarPubMed
Krach, S, Jansen, A, Krug, A, Markov, V, Thimm, M, Sheldrick, AJ, Eggermann, T, Zerres, K, Stocker, T, Shah, NJ, Kircher, T (2010). COMT genotype and its role on hippocampal-prefrontal regions in declarative memory. NeuroImage 53, 978–984.CrossRefGoogle ScholarPubMed
Krug, A, Markov, V, Krach, S, Jansen, A, Zerres, K, Eggermann, T, Stocker, T, Shah, NJ, Nothen, MM, Treutlein, J, Rietschel, M, Kircher, T (2010). The effect of Neuregulin 1 on neural correlates of episodic memory encoding and retrieval. NeuroImage 53, 985–991.CrossRefGoogle ScholarPubMed
Jansen, A, Krach, S, Krug, A, Markov, V, Thimm, M, Paulus, FM, Zerres, K, Stocker, T, Shah, NJ, Nothen, MM, Treutlein, J, Rietschel, M, Kircher, T (2010). The effect of G72 genotype on neural correlates of memory encoding and retrieval. NeuroImage 53, 1001–1006.CrossRefGoogle ScholarPubMed
Lang, PJ, Bradley, MM, Cuthbert, BN (1997). International Affective Picture System (IAPS): Technical Manual and Affective Ratings. NIMH Center for the Study of Emotion and Attention, University of Florida: Gainesville, FL.Google Scholar
Leavitt, VM, Goldberg, TE (2009). Episodic memory in schizophrenia. Neuropsychology Review 19, 312–323.CrossRefGoogle ScholarPubMed
Lepage, M, Sergerie, K, Pelletier, M, Harvey, PO (2007). Episodic memory bias and the symptoms of schizophrenia. Canadian Journal of Psychiatry 52, 702–709.CrossRefGoogle ScholarPubMed
Lipska, BK, Weinberger, DR (2000). To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 23, 223–229.CrossRefGoogle Scholar
MacDonald, AW 3rd, Thermenos, HW, Barch, DM, Seidman, LJ (2009). Imaging genetic liability to schizophrenia: systematic review of FMRI studies of patients' nonpsychotic relatives. Schizophrenia Bulletin 35, 1142–1162.CrossRefGoogle ScholarPubMed
Maxwell, M (1992). Family Interview for Genetic Studies (FIGS): Manual For FIGS. Clinical Neurogenetics Branch, Intramural Research Program, National Institute of Mental Health: Bethesda, MD.Google Scholar
Nelson, D (1979). Remembering pictures and words: appearance, significance and name. In Levels of Processing in Human Memory (ed. Cermak, L. and Craik, F.), pp. 45–76. Lawrence Erlbaum: Hillsdale, NJ.Google Scholar
O'Driscoll, GA, Florencio, PS, Gagnon, D, Wolff, AV, Benkelfat, C, Mikula, L, Lal, S, Evans, AC (2001). Amygdala-hippocampal volume and verbal memory in first-degree relatives of schizophrenic patients. Psychiatry Research 107, 75–85.CrossRefGoogle ScholarPubMed
Owens, SF, Picchioni, MM, Rijsdijk, FV, Stahl, D, Vassos, E, Rodger, AK, Collier, DA, Murray, RM, Toulopoulou, T (2011). Genetic overlap between episodic memory deficits and schizophrenia: results from the Maudsley Twin Study. Psychological Medicine 41, 521–532.CrossRefGoogle ScholarPubMed
Ranganath, C, Minzenberg, MJ, Ragland, JD (2008). The cognitive neuroscience of memory function and dysfunction in schizophrenia. Biological Psychiatry 64, 18–25.CrossRefGoogle ScholarPubMed
Schacter, DL, Wagner, AD (1999). Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 9, 7–24.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Seidman, LJ, Faraone, SV, Goldstein, JM, Kremen, WS, Horton, NJ, Makris, N, Toomey, R, Kennedy, D, Caviness, VS, Tsuang, MT (2002). Left hippocampal volume as a vulnerability indicator for schizophrenia: a magnetic resonance imaging morphometric study of nonpsychotic first-degree relatives. Archives of General Psychiatry 59, 839–849.CrossRefGoogle ScholarPubMed
Snitz, BE, MacDonald, AW 3rd, Carter, CS (2006). Cognitive deficits in unaffected first-degree relatives of schizophrenia patients: a meta-analytic review of putative endophenotypes. Schizophrenia Bulletin 32, 179–194.CrossRefGoogle ScholarPubMed
Squire, LR, Stark, CE, Clark, RE (2004). The medial temporal lobe. Annual Review of Neuroscience 27, 279–306.CrossRefGoogle ScholarPubMed
Tamminga, CA, Thomas, BP, Chin, R, Mihalakos, P, Youens, K, Wagner, AD, Preston, AR (2012). Hippocampal novelty activations in schizophrenia: disease and medication effects. Schizophrenia Research 138, 157–163.CrossRefGoogle ScholarPubMed
Thermenos, HW, Seidman, LJ, Poldrack, RA, Peace, NK, Koch, JK, Faraone, SV, Tsuang, MT (2007). Elaborative verbal encoding and altered anterior parahippocampal activation in adolescents and young adults at genetic risk for schizophrenia using FMRI. Biological Psychiatry 61, 564–574.CrossRefGoogle Scholar
Thimm, M, Krug, A, Markov, V, Krach, S, Jansen, A, Zerres, K, Eggermann, T, Stocker, T, Shah, NJ, Nothen, MM, Rietschel, M, Kircher, T (2010). The impact of dystrobrevin-binding protein 1 (DTNBP1) on neural correlates of episodic memory encoding and retrieval. Human Brain Mapping 31, 203–209.CrossRefGoogle ScholarPubMed
Toulopoulou, T, Goldberg, TE, Mesa, IR, Picchioni, M, Rijsdijk, F, Stahl, D, Cherny, SS, Sham, P, Faraone, SV, Tsuang, M, Weinberger, DR, Seidman, LJ, Murray, RM (2010). Impaired intellect and memory: a missing link between genetic risk and schizophrenia? Archives of General Psychiatry 67, 905–913.CrossRefGoogle ScholarPubMed
Toulopoulou, T, Morris, RG, Rabe-Hesketh, S, Murray, RM (2003 a). Selectivity of verbal memory deficit in schizophrenic patients and their relatives. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics 116B, 1–7.CrossRefGoogle ScholarPubMed
Toulopoulou, T, Picchioni, M, Rijsdijk, F, Hua-Hall, M, Ettinger, U, Sham, P, Murray, R (2007). Substantial genetic overlap between neurocognition and schizophrenia: genetic modeling in twin samples. Archives of General Psychiatry 64, 1348–1355.CrossRefGoogle ScholarPubMed
Toulopoulou, T, Rabe-Hesketh, S, King, H, Murray, RM, Morris, RG (2003 b). Episodic memory in schizophrenic patients and their relatives. Schizophrenia Research 63, 261–271.CrossRefGoogle ScholarPubMed
Tulving, E (1983). Elements of Episodic Memory. Oxford University Press: New York.Google Scholar
Wagner, AD, Poldrack, RA, Eldridge, LL, Desmond, JE, Glover, GH, Gabrieli, JD (1998). Material-specific lateralization of prefrontal activation during episodic encoding and retrieval. Neuroreport 9, 3711–3717.CrossRefGoogle ScholarPubMed
Wechsler, D (1954). A standardized memory scale for clinical use. Journal of Psychology 19, 87–95.CrossRefGoogle Scholar
Weinberger, DR (1999). Cell biology of the hippocampal formation in schizophrenia. Biological Psychiatry 45, 395–402.CrossRefGoogle ScholarPubMed
Whyte, MC, Whalley, HC, Simonotto, E, Flett, S, Shillcock, R, Marshall, I, Goddard, NH, Johnstone, EC, Lawrie, SM (2006). Event-related fMRI of word classification and successful word recognition in subjects at genetically enhanced risk of schizophrenia. Psychological Medicine 36, 1427–1439.CrossRefGoogle ScholarPubMed
Wright, IC, Rabe-Hesketh, S, Woodruff, PW, David, AS, Murray, RM, Bullmore, ET (2000). Meta-analysis of regional brain volumes in schizophrenia. American Journal of Psychiatry 157, 16–25.CrossRefGoogle ScholarPubMed
Supplementary material: File

Giorgio Supplementary Material

Appendix

Download Giorgio Supplementary Material(File)
File 13.4 KB