Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-04T20:09:10.851Z Has data issue: false hasContentIssue false
  • English
  • Français

A functional MRI study of verbal fluency in adults with bipolar disorder and their unaffected relatives

Published online by Cambridge University Press:  11 February 2010

M. P. G. Allin ,
N. Marshall ,
K. Schulze ,
M. Walshe ,
M.-H. Hall ,
M. Picchioni ,
R. M. Murray  and
C. McDonald
M. P. G. Allin*
Affiliation:
King's College London, Institute of Psychiatry, Department of Psychological Medicine and Psychiatry, London, UK
N. Marshall
Affiliation:
King's College London, Institute of Psychiatry, Department of Psychological Medicine and Psychiatry, London, UK
K. Schulze
Affiliation:
King's College London, Institute of Psychiatry, Department of Psychological Medicine and Psychiatry, London, UK
M. Walshe
Affiliation:
King's College London, Institute of Psychiatry, Department of Psychological Medicine and Psychiatry, London, UK
M.-H. Hall
Affiliation:
Psychology Research Laboratory, Harvard Medical School, McLean Hospital, Belmont, MA, USA
M. Picchioni
Affiliation:
King's College London, Institute of Psychiatry, Department of Psychological Medicine and Psychiatry, London, UK
R. M. Murray
Affiliation:
King's College London, Institute of Psychiatry, Department of Psychological Medicine and Psychiatry, London, UK
C. McDonald
Affiliation:
Department of Psychiatry, National University of Ireland, Galway, Galway, Republic of Ireland
*
*Address for correspondence: Dr M. P. G. Allin, Box 63, Institute of Psychiatry, De Crespigny Park, London SE5 8AF, UK. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Individuals with a history of bipolar disorder demonstrate abnormalities of executive function, even during euthymia. The neural architecture underlying this and its relationship with genetic susceptibility for illness remain unclear.

Method

We assessed 18 remitted individuals with bipolar disorder, 19 of their unaffected first degree relatives and 19 healthy controls using functional magnetic resonance imaging (fMRI) and a paced verbal fluency task with two levels of difficulty.

Results

Bipolar patients made significantly more errors in the easy level of the verbal fluency task than their relatives or controls. Analysis of variance of fMRI data demonstrated a significant main effect of group in a large cluster including retrosplenial cortex and adjacent precuneate cortex (x=7, y=−56, x=15). All three groups showed deactivation in these areas during task performance relative to a neutral or rest condition. Group differences comprised a lesser amount of deactivation in unaffected relatives compared with controls in the easy condition [F(2, 55)=3.42, p=0.04] and in unaffected relatives compared with bipolar patients in the hard condition [F(2, 55)=4.34, p=0.018]. Comparison with the control group indicated that both bipolar patients and their relatives showed similar deficits of deactivation in retrosplenial cortex and reduced activation of left prefrontal cortex.

Conclusions

Bipolar disorder may be associated with an inherited abnormality of a neural network incorporating left prefrontal cortex and bilateral retrosplenial cortex.

Keywords

Bipolar affective disordercognitionfMRI
Type
Original Articles
Information
Psychological Medicine , Volume 40 , Issue 12 , December 2010 , pp. 2025 - 2035
Copyright
Copyright © Cambridge University Press 2010

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

Altman, EG, Hedeker, D, Peterson, JL, Davis, JM (1997). The Altman Self-Rating Mania Scale. Biological Psychiatry 42, 948–955.CrossRefGoogle ScholarPubMed
Amunts, K, Weiss, PH, Mohlberg, H, Pieperhoff, P, Eickhoff, S, Gurd, JM, Marshall, JC, Shah, NJ, Fink, GR, Zilles, K (2004). Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space – the roles of Brodmann areas 44 and 45. NeuroImage 22, 42–56.CrossRefGoogle ScholarPubMed
Andreasen, NC, O‘Leary, DS, Flaum, M, Nopoulos, P, Watkins, GL, Boles Ponto, LL, Hichwa, RD (1997). Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naïve patients. Lancet 349, 1730–1734.CrossRefGoogle ScholarPubMed
Arts, B, Jabben, N, Krabbendam, L, van Os, J (2008). Meta-analyses of cognitive functioning in euthymic bipolar patients and their first-degree relatives. Psychological Medicine 38, 771–785.CrossRefGoogle ScholarPubMed
Balanza-Martınez, V, Rubio, C, Selva-Vera, G, Anabel Martinez-Aran, A, Sánchez-Moreno, J, Salazar-Fraile, J, Eduard Vieta, E, Tabares-Seisdedos, R (2008). Neurocognitive endophenotypes (Endophenocognitypes) from studies of relatives of bipolar disorder subjects: A systematic review. Neuroscience and Biobehavioral Reviews 32, 1426–1438.CrossRefGoogle ScholarPubMed
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–571.CrossRefGoogle ScholarPubMed
Blumberg, HP, Stern, E, Martinez, D, Ricketts, S, de Asis, J, White, T, Epstein, J, McBride, PA, Eidelberg, D, Kocsis, JH, Silbersweig, DA (2000). Increased anterior cingulate and caudate activity in bipolar mania. Biological Psychiatry 48, 1045–1052.CrossRefGoogle ScholarPubMed
Bora, E, Vahip, S, Akdeniz, F, İlerisoy, H, Aldemir, E, Alkan, M (2008). Executive and verbal working memory dysfunction in first-degree relatives of patients with bipolar disorder. Psychiatry Research 161, 318–324.CrossRefGoogle ScholarPubMed
Bora, E, Yucel, M, Pantelis, C (2009). Cognitive endophenotypes of bipolar disorder: a meta-analysis of neuropsychological deficits in euthymic patients and their first-degree relatives. Journal of Affective Disorders 113, 1–20.CrossRefGoogle ScholarPubMed
Brammer, MJ, Bullmore, ET, Simmons, A, Williams, SC, Grasby, PM, Howard, RJ, woodruff, PW, Rabe-Hesketh, S (1997). Generic brain activation mapping in functional magnetic resonance imaging, a nonparametric approach. Magnetic Resonance Imaging 15, 763–770.CrossRefGoogle ScholarPubMed
Bullmore, ET, Long, C, Suckling, J, Fadili, J, Calvert, GA, Zelaya, F, Carpenter, TA, Brammer, MJ (2001). Colored noise and computational inference in neurophysiological (fMRI) time series analysis: resampling methods in time and wavelet domains. Human Brain Mapping 12, 61–78.3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Bullmore, ET, Suckling, J, Overmeyer, S, Rabe-Hesketh, S, Taylor, E, Brammer, MJ (1999). Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Transactions on Medical Imaging 18, 32–42.CrossRefGoogle ScholarPubMed
Caligiuri, MP, Brown, GG, Meloy, MJ, Eberson, SC, Kindermann, SS, Frank, LR, Zorrilla, LE, Lohr, JB (2003). An fMRI study of affective state and medication on cortical and subcortical brain regions during motor performance in bipolar disorder. Psychiatry Research 123, 171–182.CrossRefGoogle ScholarPubMed
Carlson, P, Singh, J, Zarate, C Jr., Drevets, W, Manji, H (2006). Neural circuitry and neuroplasticity in mood disorders: Insights for novel therapeutic targets. NeuroRX 3, 22–41.CrossRefGoogle ScholarPubMed
Cavanagh, JTO, Van Beck, M, Muir, W, Blackwood, DHR (2001). Case-control study of neurocognitive function in euthymic patients with bipolar disorder, an association with mania. British Journal of Psychiatry 180, 320–326.CrossRefGoogle Scholar
Chaddock, CA, Barker, GJ, Marshall, N, Schulze, K, Hall, MH, Fern, A, Walshe, M, Bramon, E, Chitnis, XA, Murray, RM, McDonald, C (2009). White matter tract microstructure in patients with familial bipolar I disorder and their unaffected relatives, a diffusion tensor imaging study. British Journal of Psychiatry 194, 527–534.CrossRefGoogle Scholar
Curtis, VA, Dixon, TA, Morris, RG, Bullmore, ET, Brammer, MJ, Williams, SC, Sharma, T, Murray, RM, McGuire, PK (2001). Differential frontal activation in schizophrenia and bipolar illness during verbal fluency. Journal of Affective Disorders 66, 111–121.CrossRefGoogle ScholarPubMed
Curtis, VA, Thompson, JM, Seal, ML, Monks, PJ, Lloyd, AJ, Harrison, L, Brammer, MJ, Williams, SCR, Murray, RM, Young, AH, Ferrier, IN (2007). The nature of abnormal language processing in euthymic bipolar I disorder: evidence for a relationship between task demand and prefrontal function. Bipolar Disorders 9, 358–369.CrossRefGoogle ScholarPubMed
Drapier, D, Surguladze, S, Marshall, N, Schulze, K, Fern, A, Hall, M-H, Walshe, M, Murray, RM, McDonald, C (2008). Genetic liability for bipolar disorder is characterised by excess frontal activation in response to a working memory task. Biological Psychiatry 64, 513–520.CrossRefGoogle ScholarPubMed
Endicott, J, Spitzer, RL (1978). A diagnostic interview, the schedule for affective disorders and schizophrenia. Archives of General Psychiatry 35, 837–844.CrossRefGoogle ScholarPubMed
Fair, DA, Cohen, AL, Dosenbach, NUF, Church, JA, Miezin, FM, Barch, DM (2008). The maturing architecture of the brain's default network. Proceedings of the National Academy of Sciences 105, 4028–4032.CrossRefGoogle ScholarPubMed
Fletcher, PC, Frith, CD, Baker, SC, Shallice, T, Frackowiak, RSJ, Dolan, RJ (1995). The minds eye-activation of the precuneus in memory related imagery. Neuroimage 2, 196–200.CrossRefGoogle ScholarPubMed
Friedman, JNW, Hurley, RA, Taber, KH (2006). Bipolar disorder, imaging state versus trait. Journal of Neuropsychiatry and Clinical Neuroscience 18, 296–301.CrossRefGoogle ScholarPubMed
Fu, CHY, Morgan, K, Suckling, J, Williams, SCR, Andrew, C, Vythelingum, GN, McGuire, PK (2002). A functional magnetic resonance imaging study of overt letter verbal fluency using a clustered acquisition sequence, Greater anterior cingulate activation with increased task demand. NeuroImage 17, 871–879.CrossRefGoogle ScholarPubMed
Fu, CHY, Suckling, J, Williams, SCR, Andrew, CM, Vythelingum, GN, McGuire, PK (2005). Effects of psychotic state and task demand on prefrontal function in schizophrenia: an fMRI study of overt verbal fluency. American Journal of Psychiatry 162, 485–494.CrossRefGoogle ScholarPubMed
Ho, AP, Gillin, JC, Buchsbaum, MS, Wu, JC, Abel, L, Bunney, WE Jr. (1996). Brain glucose metabolism during non-rapid eye movement sleep in major depression. A positron emission tomography study. Archives of General Psychiatry 53, 645–652.CrossRefGoogle ScholarPubMed
Hoffman, RE, Stopek, S, Andreasen, NC (1986). A comparative study of manic vs schizophrenic speech disorganization. Archives of General Psychiatry 43, 831–838.CrossRefGoogle ScholarPubMed
Kendler, KS (2003). The genetics of schizophrenia, Chromosomal deletions, attentional disturbances, and spectrum boundaries. American Journal of Psychiatry 160, 1549–1553.CrossRefGoogle ScholarPubMed
McDonald, C, Marshall, N, Sham, PC, Bullmore, ET, Schulze, K, Chapple, B, Bramon, E, Filbey, F, Quraishi, S, Walshe, M, Murray, RM (2006). Regional brain morphometry in patients with schizophrenia or bipolar disorder and their unaffected relatives. American Journal of Psychiatry 163, 478–487.CrossRefGoogle ScholarPubMed
McIntosh, AM, Heather, WC, 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, 378–384.CrossRefGoogle Scholar
Maddock, RJ (2000). The retrosplenial cortex and emotion, new insights from functional neuroimaging of the human brain. Trends in Neurosciences 22, 310–316.CrossRefGoogle Scholar
Maddock, RJ, Garrett, AS, Buonocore, MH (2003). Posterior cingulate cortex activation by emotional words, fMRI evidence from a valence decision task. Human Brain Mapping 18, 30–41.CrossRefGoogle ScholarPubMed
Martínez-Arán, A, Vieta, E, Reinares, M, Colom, F, Torrent, C, Sánchez-Moreno, J, Benabarre, A, Goikolea, JM, Comes, M, Salamero, M (2004). Cognitive function across manic or hypomanic, depressed, and euthymic states in bipolar disorder. American Journal of Psychiatry 161, 262–270.CrossRefGoogle ScholarPubMed
Mesulam, M-M (2000). Behavioral neuroanatomy, large-scale networks, association cortex, frontal syndromes, the limbic system, and hemispheric specializations. In Principles of Behavioral and Cognitive Neurology (ed. Mesulam, M.-M.), pp. 1–120. Oxford University Press: Oxford.CrossRefGoogle Scholar
Monks, PJ, Thompson, JM, Bullmore, ET, Suckling, J, Brammer, MJ, Williams, SCR, 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, 550–564.CrossRefGoogle ScholarPubMed
Murphy, FC, Sahakian, BJ (2001). Neuropsychology of bipolar disorder. British Journal of Psychiatry 178, s120–s127.CrossRefGoogle ScholarPubMed
Nugent, AC, Milham, MP, Bain, EE (2006). Cortical abnormalities in bipolar disorder investigated with MRI and voxel-based morphometry. Neuroimage 30, 485–497.CrossRefGoogle ScholarPubMed
Reed, LJ, Lasserson, D, Marsden, P, Bright, P, Nicola, S, Kopelman, MD (2005). Correlations of regional cerebral metabolism with memory performance and executive function in patients with herpes encephalitis or frontal lobe lesions. Neuropsychology 19, 555–565.CrossRefGoogle ScholarPubMed
Robinson, LJ, Thompson, JM, Gallagher, P, Goswami, U, Young, AH, Ferrier, IN, Moore, PB (2006). A meta-analysis of cognitive deficits in euthymic patients with bipolar disorder. Journal of Affective Disorders 93, 105–115.CrossRefGoogle ScholarPubMed
Sassi, RB, Brambilla, P, Hatch, JP, Nicoletti, MA, Mallinger, AG, Frank, E, Kupfer, DJ, Keshavan, MS, Soares, JC (2004). Reduced left anterior cingulate volumes in untreated bipolar patients. Biological Psychiatry 56, 467–475.CrossRefGoogle ScholarPubMed
Schlösser, R, Hutchinson, M, Joseffer, S, Rusinek, H, Saarimaki, A, Stevenson, J, Dewey, SL, Brodie, JD (1998). Functional magnetic resonance imaging of human brain activity in a verbal fluency task. Journal of Neurology, Neurosurgery and Psychiatry 64, 492–498.CrossRefGoogle Scholar
Sonuga-Barke, EJS, Castellanos, FX (2007). Spontaneous attentional fluctuations in impaired states and pathological conditions, a neurobiological hypothesis. Neuroscience & Biobehavioral Reviews 31, 977–986.CrossRefGoogle ScholarPubMed
Strakowski, SM, DelBello, MP, Adler, CM (2005). The functional neuroanatomy of bipolar disorder, a review of neuroimaging findings. Molecular Psychiatry 10, 105–116.CrossRefGoogle ScholarPubMed
Strakowski, SM, DelBello, MP, Adler, C, Cecil, KM, Sax, KW (2000). Neuroimaging in bipolar disorder. Bipolar Disorders 2, 148–164.CrossRefGoogle ScholarPubMed
Strauss, E, Sherman, E, Spreen, O (2006). A Compendium of Neuropsychological Tests, Administration, Norms and Commentary, 3rd edn. Oxford University Press: London.Google Scholar
Torrent, C, Martinez-Arán, A, Daban, C, Sanchez-Moreno, J, Comes, M, Goikolea, JM, Salamero, M, Vieta, E (2006). Cognitive impairment in bipolar II disorder. British Journal of Psychiatry 189, 254–259.CrossRefGoogle ScholarPubMed
Yoshimura, H, Sugai, T, Honjo, M, Segami, N, Onoda, N (2005). NMDA receptor-dependent oscillatory signal outputs from the retrosplenial cortex triggered by a non-NMDA receptor-dependent signal input from the visual cortex. Brain Research 1045, 12–21.CrossRefGoogle ScholarPubMed
Zubieta, J-K, Huguelet, P, O'Neil, RN, Giordani, BJ (2001). Cognitive function in euthymic bipolar I disorder. Psychiatry Research 102, 9–20.CrossRefGoogle ScholarPubMed