Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-20T17:36:25.091Z Has data issue: false hasContentIssue false

Hippocampal function in schizophrenia and bipolar disorder

Published online by Cambridge University Press:  07 September 2009

J. Hall*
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
H. C. Whalley
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
K. Marwick
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
J. McKirdy
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
J. Sussmann
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
L. Romaniuk
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
E. C. Johnstone
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
H. I. Wan
Affiliation:
Clinical Translational Medicine, Wyeth Research, Collegeville, PA, USA
A. M. McIntosh
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
S. M. Lawrie
Affiliation:
Division of Psychiatry, University of Edinburgh, Royal Edinburgh Hospital, Edinburgh, UK
*
*Address for correspondence: Dr J. Hall, Division of Psychiatry, University of Edinburgh, Kennedy Tower, Royal Edinburgh Hospital, EdinburghEH10 5HF, UK. (Email: [email protected])

Abstract

Background

The hippocampus plays a central role in memory formation. There is considerable evidence of abnormalities in hippocampal structure and function in schizophrenia, which may differentiate it from bipolar disorder. However, no previous studies have compared hippocampal activation in schizophrenia and bipolar disorder directly.

Method

Fifteen patients with schizophrenia, 14 patients with bipolar disorder and 14 healthy comparison subjects took part in the study. Subjects performed a face–name pair memory task during functional magnetic resonance imaging (fMRI). Differences in blood oxygen level-dependent (BOLD) activity were determined during encoding and retrieval of the face–name pairs.

Results

The patient groups showed significant differences in hippocampal and prefrontal cortex (PFC) activation during face–name pair learning. During encoding, patients with schizophrenia showed decreased anterior hippocampal activation relative to subjects with bipolar disorder, whereas patients with bipolar disorder showed decreased dorsal PFC activation relative to patients with schizophrenia. During retrieval, patients with schizophrenia showed greater activation of the dorsal PFC than patients with bipolar disorder. Patients with schizophrenia also differed from healthy control subjects in the activation of several brain regions, showing impaired superior temporal cortex activation during encoding and greater dorsal PFC activation during retrieval. These effects were evident despite matched task performance.

Conclusions

Patients with schizophrenia showed deficits in hippocampal activation during a memory task relative to patients with bipolar disorder. The disorders were further distinguished by differences in PFC activation. The results demonstrate that these disorders can distinguished at a group level using non-invasive neuroimaging.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2009

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, Lepage, M (2003). Is associative recognition more impaired than item recognition memory in schizophrenia? A meta-analysis. Brain and Cognition 53, 121124.Google Scholar
Achim, AM, Lepage, M (2005). Episodic memory-related activation in schizophrenia: meta-analysis. British Journal of Psychiatry 187, 500509.CrossRefGoogle ScholarPubMed
Aleman, A, Hijman, R, de Haan, EHF, Kahn, RS (1999). Memory impairment in schizophrenia: a meta-analysis. American Journal of Psychiatry 156, 13581366.CrossRefGoogle ScholarPubMed
Blumberg, HP, Leung, H-C, Skudlarski, P, Lacadie, CM, Fredericks, CA, Harris, BC, Charney, DS, Gore, JC, Krystal, JH, Peterson, BS (2003). A functional magnetic resonance imaging study of bipolar disorder: state- and trait-related dysfunction in ventral prefrontal cortices. Archives of General Psychiatry 60, 601609.Google Scholar
Blumenfeld, RS, Ranganath, C (2007). Prefrontal cortex and long-term memory encoding: an integrative review of findings from neuropsychology and neuroimaging. Neuroscientist 13, 280291.CrossRefGoogle ScholarPubMed
Boos, HBM, Aleman, A, Cahn, W, Pol, HH, Kahn, RS (2007). Brain volumes in relatives of patients with schizophrenia: a meta-analysis. Archives of General Psychiatry 64, 297304.CrossRefGoogle ScholarPubMed
Callicott, JH, Mattay, VS, Verchinski, BA, Marenco, S, Egan, MF, Weinberger, DR (2003). Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. American Journal of Psychiatry 160, 22092215.CrossRefGoogle ScholarPubMed
Chen, C-H, Lennox, B, Jacob, R, Calder, A, Lupson, V, Bisbrown-Chippendale, R, Suckling, J, Bullmore, E (2006). Explicit and implicit facial affect recognition in manic and depressed states of bipolar disorder: a functional magnetic resonance imaging study. Biological Psychiatry 59, 3139.CrossRefGoogle ScholarPubMed
Curtis, VA, Dixon, TA, Morris, RG, Bullmore, ET, Brammer, MJ, Williams, SCR, Sharma, T, Murray, RM, McGuire, PK (2001). Differential frontal activation in schizophrenia and bipolar illness during verbal fluency. Journal of Affective Disorders 66, 111121.Google Scholar
Danion, J-M, Rizzo, L, Bruant, A (1999). Functional mechanisms underlying impaired recognition memory and conscious awareness in patients with schizophrenia. Archives of General Psychiatry 56, 639644.CrossRefGoogle ScholarPubMed
Deckersbach, T, Dougherty, DD, Savage, C, McMurrich, S, Fischman, AJ, Nierenberg, A, Sachs, G, Rauch, SL (2006). Impaired recruitment of the dorsolateral prefrontal cortex and hippocampus during encoding in bipolar disorder. Biological Psychiatry 59, 138146.Google Scholar
Dolan, RJ, Fletcher, PF (1999). Encoding and retrieval in human medial temporal lobes: an empirical investigation using functional magnetic resonance imaging (fMRI). Hippocampus 9, 2534.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Fletcher, PC, Frith, CD, Rugg, MD (1997). The functional neuroanatomy of episodic memory. Trends in Neurosciences 20, 213218.Google Scholar
Frey, BN, Andreazza, AC, Nery, FG, Martins, MR, Quevedo, J, Soares, JC, Kapczinski, F (2007). The role of hippocampus in the pathophysiology of bipolar disorder. Behavioural Pharmacology 18, 419430.CrossRefGoogle ScholarPubMed
Haldane, M, Frangou, S (2004). New insights help define the pathophysiology of bipolar affective disorder: neuroimaging and neuropathology findings. Progress in Neuro-Psychopharmacology and Biological Psychiatry 28, 943960.Google Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 5662.CrossRefGoogle ScholarPubMed
Heckers, S (2001). Neuroimaging studies of the hippocampus in schizophrenia. Hippocampus 11, 520528.Google Scholar
Heckers, S, Rauch, S, Goff, D, Savage, C, Schacter, D, Fischman, A, Alpert, N (1998). Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nature Neuroscience 1, 318323.Google Scholar
Henson, RNA, Rugg, MD, Shallice, T, Josephs, O, Dolan, RJ (1999). Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. Journal of Neuroscience 19, 39623972.CrossRefGoogle ScholarPubMed
Huron, C, Danion, JM, Giacomoni, F, Grange, D, Robert, P, Rizzo, L (1995). Impairment of recognition memory with, but not without, conscious recollection in schizophrenia. American Journal of Psychiatry 152, 17371742.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261276.CrossRefGoogle ScholarPubMed
Kirwan, CB, Stark, CE (2004). Medial temporal lobe activation during encoding and retrieval of novel face–name pairs. Hippocampus 14, 919930.Google Scholar
Lagopoulos, J, Ivanovski, B, Malhi, GS (2007). An event-related functional MRI study of working memory in euthymic bipolar disorder. Journal of Psychiatry and Neuroscience 32, 174184.Google Scholar
Lawrence, NS, Williams, AM, Surguladze, S, Giampietro, V, Brammer, MJ, Andrew, C, Frangou, S, Ecker, C, Phillips, ML (2004). Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biological Psychiatry 55, 578587.Google Scholar
Lepage, M, Habib, R, Tulving, E (1998). Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus 8, 313322.Google Scholar
Lisman, JE, Coyle, JT, Green, RW, Javitt, DC, Benes, FM, Heckers, S, Grace, AA (2008). Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends in Neurosciences 31, 234242.Google Scholar
Lodge, DJ, Grace, AA (2007). Aberrant hippocampal activity underlies the dopamine dysregulation in an animal model of schizophrenia. Journal of Neuroscience 27, 1142411430.Google Scholar
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19, 12331239.Google Scholar
Mayes, A, Montaldi, D, Migo, E (2007). Associative memory and the medial temporal lobes. Trends in Cognitive Sciences 11, 126135.Google Scholar
McIntosh, AM, Whalley, HC, McKirdy, J, Hall, J, Sussmann, JED, Shankar, P, Johnstone, EC, Lawrie, SM (2008). Prefrontal function and activation in bipolar disorder and schizophrenia. American Journal of Psychiatry 165, 378384.CrossRefGoogle Scholar
Monks, PJ, Thompson, JM, Bullmore, ET, Suckling, J, Brammer, MJ, Williams, SC, Simmons, A, Giles, N, Lloyd, AJ, Harrison, CL, Seal, M, Murray, RM, Ferrier, IN, Young, AH, Curtis, VA (2004). A functional MRI study of working memory task in euthymic bipolar disorder: evidence for task-specific dysfunction. Bipolar Disorders 6, 550564.Google Scholar
Nelson, HE, Willison, JR (1991). The Revised National Adult Reading Test – Test Manual. NFER-Nelson: Windsor, UK.Google Scholar
Ongur, D, Cullen, TJ, Wolf, DH, Rohan, M, Barreira, P, Zalesak, M, Heckers, S (2006). The neural basis of relational memory deficits in schizophrenia. Archives of General Psychiatry 63, 356365.CrossRefGoogle ScholarPubMed
Phillips, ML, Vieta, E (2007). Identifying functional neuroimaging biomarkers of bipolar disorder: toward DSM-V. Schizophrenia Bulletin 33, 893904.CrossRefGoogle ScholarPubMed
Sperling, R, Chua, E, Cocchiarella, A, Rand-Giovannetti, E, Poldrack, R, Schacter, DL, Albert, M (2003). Putting names to faces: successful encoding of associative memories activates the anterior hippocampal formation. NeuroImage 20, 14001410.Google Scholar
Strakowski, SM, DelBello, MP, Adler, CM (2004). The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Molecular Psychiatry 10, 105116.Google Scholar
Summerfield, C, Greene, M, Wager, T, Egner, T, Hirsch, J, Mangels, J (2006). Neocortical connectivity during episodic memory formation. PLoS Biology 4, e128.Google Scholar
Toulopoulou, T, Rabe-Hesketh, S, King, H, Murray, RM, Morris, RG (2003). Episodic memory in schizophrenic patients and their relatives. Schizophrenia Research 63, 261271.Google Scholar
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273289.Google Scholar
Vargha-Khadem, F, Gadian, DG, Watkins, KE, Connelly, A, Van Paesschen, W, Mishkin, M (1997). Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376380.CrossRefGoogle ScholarPubMed
Woods, SW (2003). Chlorpromazine equivalent doses of the newer atypical antipsychotics. Journal of Clinical Psychiatry 64, 663667.CrossRefGoogle ScholarPubMed
Wright, IC, Rabe-Hesketh, S, Woodruff, PWR, David, AS, Murray, RM, Bullmore, ET (2000). Meta-analysis of regional brain volumes in schizophrenia. American Journal of Psychiatry 157, 1625.Google Scholar
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429435.Google Scholar
Zeineh, MM, Engel, SA, Thompson, PM, Bookheimer, SY (2003). Dynamics of the hippocampus during encoding and retrieval of face–name pairs. Science 299, 577580.Google Scholar
Supplementary material: File

Hall supplementary material

Tables.doc

Download Hall supplementary material(File)
File 158.6 KB