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Prefrontal hypoactivation during working memory in bipolar II depression

Published online by Cambridge University Press:  10 March 2015

J. O. Brooks III*
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, UCLA Semel Institute for Neuroscience & Human Behavior, Los Angeles, CA, USA
N. Vizueta
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, UCLA Semel Institute for Neuroscience & Human Behavior, Los Angeles, CA, USA
C. Penfold
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, UCLA Semel Institute for Neuroscience & Human Behavior, Los Angeles, CA, USA
J. D. Townsend
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, UCLA Semel Institute for Neuroscience & Human Behavior, Los Angeles, CA, USA
S. Y. Bookheimer
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, UCLA Semel Institute for Neuroscience & Human Behavior, Los Angeles, CA, USA
L. L. Altshuler
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, UCLA Semel Institute for Neuroscience & Human Behavior, Los Angeles, CA, USA
*
* Address for correspondence: J. O. Brooks, Ph.D., M.D., Department of Psychiatry & Biobehavioral Sciences, UCLA Semel Institute for Neuroscience & Human Behavior, 300 Medical Plaza, Suite 2229, Los Angeles, CA 90024, USA. (Email: [email protected])

Abstract

Background.

Patterns of abnormal neural activation have been observed during working memory tasks in bipolar I depression, yet the neural changes associated with bipolar II depression have yet to be explored.

Method.

An n-back working memory task was administered during a 3T functional magnetic resonance imaging scan in age- and gender-matched groups of 19 unmedicated, bipolar II depressed subjects and 19 healthy comparison subjects. Whole-brain and region-of-interest analyses were performed to determine regions of differential activation across memory-load conditions (0-, 1- and 2-back).

Results.

Accuracy for all subjects decreased with higher memory load, but there was no significant group × memory load interaction. Random-effects analyses of memory load indicated that subjects with bipolar II depression exhibited significantly less activation than healthy subjects in left hemispheric regions of the middle frontal gyrus [Brodmann area (BA) 11], superior frontal gyrus (BA 10), inferior parietal lobule (BA 40), middle temporal gyrus (BA 39) and bilateral occipital regions. There was no evidence of differential activation related to increasing memory load in the dorsolateral prefrontal or anterior cingulate cortex.

Conclusions.

Bipolar II depression is associated with hypoactivation of the left medio-frontal and parietal cortex during working memory performance. Our findings suggest that bipolar II depression is associated with disruption of the fronto-parietal circuit that is engaged in working memory tasks, which is a finding reported across bipolar subtypes and mood states.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2015 

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References

Altshuler, L, Bookheimer, S, Townsend, J, Proenza, MA, Sabb, F, Mintz, J, Cohen, MS (2008). Regional brain changes in bipolar I depression: a functional magnetic resonance imaging study. Bipolar Disorders 10, 708717.CrossRefGoogle ScholarPubMed
Bearden, CE, Shih, VH, Green, MF, Gitlin, M, Sokolski, KN, Levander, E, Marusak, S, Hammen, C, Sugar, CA, Altshuler, LL (2011). The impact of neurocognitive impairment on occupational recovery of clinically stable patients with bipolar disorder: a prospective study. Bipolar Disorders 13, 323333.CrossRefGoogle ScholarPubMed
Beckmann, CF, Jenkinson, M, Smith, SM (2003). General multilevel linear modeling for group analysis in fMRI. NeuroImage 20, 10521063.CrossRefGoogle Scholar
Bertocci, MA, Bebko, GM, Mullin, BC, Langenecker, SA, Ladouceur, CD, Almeida, JRC, Phillips, ML (2012). Abnormal anterior cingulate cortical activity during emotional n-back task performance distinguishes bipolar from unipolar depressed females. Psychological Medicine 42, 14171428.CrossRefGoogle ScholarPubMed
Braver, TS, Cohen, JD, Nystrom, LE, Jonides, J, Smith, EE, Noll, DC (1997). A parametric study of prefrontal cortex involvement in human working memory. NeuroImage 5, 4962.Google Scholar
Cabeza, R, Nyberg, L (2000). Neural bases of learning and memory: functional neuroimaging evidence. Current Opinion in Neurology 13, 415421.Google Scholar
Cohen, JD, Perlstein, WM, Braver, TS, Nystrom, LE, Noll, DC, Jonides, J, Smith, EE (1997). Temporal dynamics of brain activation during a working memory task. Nature 386, 604608.Google Scholar
Cremaschi, L, Penzo, B, Palazzo, M, Dobrea, C, Cristoffanini, M, Dell'Osso, B, Altamura, AC (2013). Assessing working memory via n-back task in euthymic bipolar I disorder patients: a review of functional magnetic resonance imaging studies. Neuropsychobiology 68, 6370.Google Scholar
Curtis, CE (2006). Prefrontal and parietal contributions to spatial working memory. Neuroscience 139, 173180.Google Scholar
Deckersbach, T, Rauch, SL, Buhlmann, U, Ostacher, MJ, Beucke, J-C, Nierenberg, AA, Sachs, G, Dougherty, DD (2008). An fMRI investigation of working memory and sadness in females with bipolar disorder: a brief report. Bipolar Disorders 10, 928942.Google Scholar
Dittmann, S, Hennig-Fast, K, Gerber, S, Seemuller, F, Riedel, M, Emanuel Severus, W, Langosch, J, Engel, RR, Moller, HJ, Grunze, HC (2008). Cognitive functioning in euthymic bipolar I and bipolar II patients. Bipolar Disorders 10, 877887.Google Scholar
Drevets, WC (1999). Prefrontal cortical–amygdalar metabolism in major depression. Annals of the New York Academy of Sciences 877, 614637.CrossRefGoogle ScholarPubMed
Fernandez-Corcuera, P, Salvador, R, Monte, GC, Salvador Sarro, S, Goikolea, JM, Amann, B, Moro, N, Sans-Sansa, B, Ortiz-Gil, J, Vieta, E, Maristany, T, McKenna, PJ, Pomarol-Clotet, E (2013). Bipolar depressed patients show both failure to activate and failure to de-activate during performance of a working memory task. Journal of Affective Disorders 148, 170178.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, J (2002). Structured Clinical Interview for DSM-IV TR Axis I Disorders. Research Version, Patient Edition (SCID-I/P). Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Fitzgerald, PB, Srithiran, A, Benitez, J, Daskalakis, ZZ, Oxley, TJ, Kulkarni, J, Egan, GF (2008). An fMRI study of prefrontal brain activation during multiple tasks in patients with major depressive disorder. Human Brain Mapping 29, 490501.Google Scholar
Garrett, A, Kelly, R, Gomez, R, Keller, J, Schatzberg, AF, Reiss, AL (2011). Aberrant brain activation during a working memory task in psychotic major depression. American Journal of Psychiatry 168, 173182.Google Scholar
Godard, J, Grondin, S, Baruch, P, Lafleur, MF (2011). Psychosocial and neurocognitive profiles in depressed patients with major depressive disorder and bipolar disorder. Psychiatry Research 190, 244252.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 5662.Google Scholar
Harvey, P-O, Fossati, P, Pochon, J-B, Levy, R, Lebastard, G, Lehéricy, S, Allilaire, J-F, Dubois, B (2005). Cognitive control and brain resources in major depression: an fMRI study using the n-back task. NeuroImage 26, 860869.CrossRefGoogle ScholarPubMed
Hsiao, YL, Wu, YS, Wu, JY, Hsu, MH, Chen, HC, Lee, SY, Lee, IH, Yeh, TL, Yang, YK, Ko, HC, Lu, RB (2009). Neuropsychological functions in patients with bipolar I and bipolar II disorder. Bipolar Disorders 11, 547554.Google Scholar
Hyler, SE, Skodol, AE, Kellman, HD, Oldham, JM, Rosnick, L (1990). Validity of the Personality Diagnostic Questionnaire – revised: comparison with two structured interviews. American Journal of Psychiatry 147, 10431048.Google ScholarPubMed
Jenkinson, M, Bannister, P, Brady, M, Smith, S (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17, 825841.Google Scholar
Jenkinson, M, Smith, S (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis 5, 143156.Google Scholar
Kammer, T, Bellemann, ME, Guckel, F, Brix, G, Gass, A, Schlemmer, H, Spitzer, M (1997). Functional MR imaging of the prefrontal cortex: specific activation in a working memory task. Magnetic Resonance Imaging 15, 879889.Google Scholar
Keilp, JG, Gorlyn, M, Russell, M, Oquendo, MA, Burke, AK, Harkavy-Friedman, J, Mann, JJ (2013). Neuropsychological function and suicidal behavior: attention control, memory and executive dysfunction in suicide attempt. Psychological Medicine 43, 539551.Google Scholar
Kriegeskorte, N, Simmons, WK, Bellgowan, PS, Baker, CI (2009). Circular analysis in systems neuroscience: the dangers of double dipping. Nature Neuroscience 12, 535540.Google Scholar
Malhi, GS, Ivanovski, B, Hadzi-Pavlovic, D, Mitchell, PB, Vieta, E, Sachdev, P (2007). Neuropsychological deficits and functional impairment in bipolar depression, hypomania and euthymia. Bipolar Disorders 9, 114125.CrossRefGoogle ScholarPubMed
Matsuo, K, Glahn, DC, Peluso, MAM, Hatch, JP, Monkul, ES, Najt, P, Sanches, M, Zamarripa, F, Li, J, Lancaster, JL, Fox, PT, Gao, J-H, Soares, JC (2007). Prefrontal hyperactivation during working memory task in untreated individuals with major depressive disorder. Molecular Psychiatry 12, 158166.Google Scholar
McKenna, BS, Sutherland, AN, Legenkaya, AP, Eyler, LT (2014). Abnormalities of brain response during encoding into verbal working memory among euthymic patients with bipolar disorder. Bipolar Disorders 16, 289299.Google 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.CrossRefGoogle ScholarPubMed
Murphy, FC, Sahakian, BJ, Rubinsztein, JS, Michael, A, Rogers, RD, Robbins, TW, Paykel, ES (1999). Emotional bias and inhibitory control processes in mania and depression. Psychological Medicine 29, 13071321.Google Scholar
Naghavi, HR, Nyberg, L (2005). Common fronto-parietal activity in attention, memory, and consciousness: shared demands on integration? Consciousness and Cognition 14, 390425.Google Scholar
Ochsner, KN, Bunge, SA, Gross, JJ, Gabrieli, JD (2002). Rethinking feelings: an fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience 14, 12151229.Google Scholar
Oishi, K, Faria, AV, van Zijl, P, Mori, S (2011). MRI Atlas of Human White Matter, 2nd edn. Academic Press: Amsterdam: The Netherlands.Google Scholar
Owen, AM, McMillan, KM, Laird, AR, Bullmore, E (2005). N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Human Brain Mapping 25, 4659.Google Scholar
Pålsson, E, Figueras, C, Johansson, AGM, Ekman, C-J, Hultman, B, Östlind, J, Landén, M (2013). Neurocognitive function in bipolar disorder: a comparison between bipolar I and II disorder and matched controls. BMC Psychiatry 13, 165.Google Scholar
Rosenthal, NE, Hefferman, ME (eds) (1987). Bulimia, Carbohydrate Craving and Depression: a Central Connection? Raven Press: New York.Google Scholar
Rush, AJ, Gullion, CM, Basco, MR, Jarrett, RB, Trivedi, MH (1996). The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychological Medicine 26, 477486.CrossRefGoogle ScholarPubMed
Schöning, S, Zwitserlood, P, Engelien, A, Behnken, A, Kugel, H, Schiffbauer, H, Lipina, K, Pachur, C, Kersting, A, Dannlowski, U, Baune, BT, Zwanzger, P, Reker, T, Heindel, W, Arolt, V, Konrad, C (2009). Working-memory fMRI reveals cingulate hyperactivation in euthymic major depression. Human Brain Mapping 30, 27462756.Google Scholar
Smith, EE, Jonides, J (1998). Neuroimaging analyses of human working memory. Proceedings of the National Academy of Sciences of the United States of America 95, 1206112068.Google Scholar
Smith, SM (2002). Fast robust automated brain extraction. Human Brain Mapping 17, 143155.Google Scholar
Sole, B, Bonnin, CM, Torrent, C, Balanza-Martinez, V, Tabares-Seisdedos, R, Popovic, D, Martinez-Aran, A, Vieta, E (2012). Neurocognitive impairment and psychosocial functioning in bipolar II disorder. Acta Psychiatrica Scandinavica 125, 309317.Google Scholar
Sole, B, Martinez-Aran, A, Torrent, C, Bonnin, CM, Reinares, M, Popovic, D, Sanchez-Moreno, J, Vieta, E (2011). Are bipolar II patients cognitively impaired? A systematic review. Psychological Medicine 41, 17911803.Google Scholar
Talairach, J, Tournoux, P (1988). Co-Planar Stereotaxic Atlas of the Human Brain: 3-D Proportional System: an Approach to Cerebral Imaging. Thieme Medical Publishers, Inc.: New York.Google Scholar
Thermenos, HW, Goldstein, JM, Milanovic, SM, Whitfield-Gabrieli, S, Makris, N, Laviolette, P, Koch, JK, Faraone, SV, Tsuang, MT, Buka, SL, Seidman, LJ (2010). An fMRI study of working memory in persons with bipolar disorder or at genetic risk for bipolar disorder. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics 153B, 120131.Google Scholar
Torrent, C, Martinez-Aran, 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, 254259.Google Scholar
Townsend, J, Bookheimer, SY, Foland-Ross, LC, Sugar, CA, Altshuler, LL (2010). fMRI abnormalities in dorsolateral prefrontal cortex during a working memory task in manic, euthymic and depressed bipolar subjects. Psychiatry Research: Neuroimaging 182, 2229.Google Scholar
Volkert, J, Kopf, J, Kazmaier, J, Glaser, F, Zierhut, KC, Schiele, MA, Kittel-Schneider, S, Reif, A (2014). Evidence for cognitive subgroups in bipolar disorder and the influence of subclinical depression and sleep disturbances. European Neuropsychopharmacology. Published online 15 08 2014 . doi:10.1016/j.euroneuro.2014.07.017.Google Scholar
Woolrich, MW, Ripley, BD, Brady, M, Smith, SM (2001). Temporal autocorrelation in univariate linear modeling of fMRI data. NeuroImage 14, 13701386.Google Scholar
Worsley, KJ (2001). Statistical analysis of activation images. In Functional MRI: An Introduction to Methods (ed Jezzard, P., Matthews, P.M. and Smith, S.M.), pp. 251270. Oxford University Press: New York.Google Scholar
Xu, G, Lin, K, Rao, D, Dang, Y, Ouyang, H, Guo, Y, Ma, J, Chen, J (2012). Neuropsychological performance in bipolar I, bipolar II and unipolar depression patients: a longitudinal, naturalistic study. Journal of Affective Disorders 136, 328339.Google Scholar
Yates, DB, Dittmann, S, Kapczinski, F, Trentini, CM (2011). Cognitive abilities and clinical variables in bipolar I depressed and euthymic patients and controls. Journal of Psychiatric Research 45, 495504.CrossRefGoogle ScholarPubMed
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429435.CrossRefGoogle ScholarPubMed