Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-05-11T06:42:15.013Z Has data issue: false hasContentIssue false
  • English
  • Français

Increased Cerebral Blood Flow Associated with Better Response Inhibition in Bipolar Disorder

Published online by Cambridge University Press:  16 March 2015

Sheena I. Dev ,
Benjamin S. McKenna ,
Ashley N. Sutherland ,
David D. Shin ,
Thomas T. Liu ,
Christina E. Wierenga  and
Lisa T. Eyler
Sheena I. Dev
Affiliation:
Research Service, Veterans Affairs, San Diego Healthcare System, San Diego, California San Diego State University/University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California Department of Psychiatry, School of Medicine, University of California, San Diego, California
Benjamin S. McKenna
Affiliation:
Department of Psychiatry, School of Medicine, University of California, San Diego, California Mental Illness Research, Education, and Clinical Center, Veterans Affairs San Diego Healthcare System, San Diego, California
Ashley N. Sutherland
Affiliation:
Research Service, Veterans Affairs, San Diego Healthcare System, San Diego, California Veterans Medical Research Foundation, San Diego, California
David D. Shin
Affiliation:
Center for Functional MRI and Department of Radiology, University of California, San Diego, California
Thomas T. Liu
Affiliation:
Center for Functional MRI and Department of Radiology, University of California, San Diego, California
Christina E. Wierenga
Affiliation:
Research Service, Veterans Affairs, San Diego Healthcare System, San Diego, California San Diego State University/University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California Department of Psychiatry, School of Medicine, University of California, San Diego, California
Lisa T. Eyler*
Affiliation:
San Diego State University/University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California Mental Illness Research, Education, and Clinical Center, Veterans Affairs San Diego Healthcare System, San Diego, California
*
Correspondence and reprint requests to: Lisa T Eyler, 3350 La Jolla Village Drive, San Diego, CA 92161 Mail Code: 151B. E-mail: lteyler@ucsd.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Impairment on inhibitory tasks has been well documented in bipolar disorder (BD). Differences in cerebral blood flow (CBF) between BD patients and healthy comparison (HC) participants have also been reported. Few studies have examined the relationship between cognitive performance and regional CBF in this patient population. We hypothesized that group differences on an inhibitory task (the Delis-Kaplan Executive Function Scale’s Color-Word Inhibition task) would be associated with differential CBF in bilateral anterior cingulate cortex (ACC), inferior parietal lobule (IPL) and dorsolateral prefrontal cortex (DLPFC) regions. Whole brain resting CBF was measured using Multiphase Pseudocontinuous Arterial Spin Labeling MR imaging for 28 euthymic BD and 36 HC participants. Total gray matter (GM) CBF was measured, and regional CBF values were extracted for each region of interest (ROI) using Freesurfer-based individual parcellations. Group, CBF, and group-by-CBF interaction were examined as predictors of inhibition performance. Groups did not differ in age, gender or education. BD patients performed significantly worse on Color-Word inhibition. There were no significant group differences in CBF in either total GM or in any ROI. There was a group by CBF interaction in the bilateral ACC, right IPL and right DLPFC such that better inhibitory performance was generally associated with higher resting state CBF in BD subjects, but not HC participants. Although CBF was not abnormal in this euthymic BD sample, results confirm previous reports of inter-episode inhibitory deficits and indicate that the perfusion-cognition relationship is different in BD compared to HC individuals. (JINS, 2015, 21, 105–115)

Keywords

ASLCognitionEuthymicVascularAnterior cingulatePrefrontal
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 21 , Issue 2 , February 2015 , pp. 105 - 115
Copyright
Copyright © The International Neuropsychological Society 2015 

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

Almeida, J.R., Mourau-Miranda, J., Alzenstein, H.J., Versace, A., Kozel, F.A., Lu, H., … Phillips, M.L. (2013). Pattern recognition analysis of anterior cingulate cortex blood flow to classify depression polarity. British Journal of Psychiatry, 203, 310–311.CrossRefGoogle Scholar
Bearden, C.E., Hoffman, K.M., & Cannon, T.D. (2001). The neuropsychology and neuroanatomy of bipolar affective disorder: A critical review. Bipolar Disorders, 3(3), 106–150.Google Scholar
Benabarre, A., Vieta, E., Martinez-Aran, A., Garcia-Garcia, M., Martin, F., Lomena, F., … Valdes, M. (2005). Neuropsychological disturbances and cerebral blood flow in bipolar disorder. The Australian and New Zealand Journal of Psychiatry, 39(4), 227–234.Google Scholar
Bhardwaj, R., Chakrabarti, S., Mittal, B.R., & Sharan, P. (2010). A single photon emission computerized tomography (SPECT) study of regional cerebral blood flow in bipolar disorder. World Journal of Biological Psychiatry, 11(Pt 2), 334–343.CrossRefGoogle ScholarPubMed
Blose, M., Coad, S., Amen, D., Willeumier, K., Taylor, D., & Golden, C. (2014). C-07SPECT Imaging in adults with nicotine-related disorders. Archives of Clinical Neuropsychology, 29(6), 575.CrossRefGoogle Scholar
Blumberg, H.P., Leung, H.C., Skudlarski, P., Lacadie, C.M., Fredericks, C.A., Harris, B.C., … Peterson, B.S. (2003). A functional magnetic resonance imaging study of bipolar disorder: A state- and trait-related dysfunction in Ventral prefrontal cortices. Archives of General Psychiatry, 60(6), 601–609.Google Scholar
Bonnin, C.M., Martinez-Aran, A., Torrent, C., Pacchiarotti, I., Rosa, A.R., Franco, C., … Vieta, E. (2010). Clinical neurocognitive predictors of functional outcome in bipolar euthymic patients: A long-term, follow up study. Journal of Affective Disorders, 121(1–2), 156–160.CrossRefGoogle ScholarPubMed
Bourne, C., Aydemir, O., Balanza-Martinez, V., Bora, E., Brissos, S., Cavanagh, J.T., … Goodwin, G.M. (2013). Neuropsychological testing of cognitive impairment in euthymic bipolar disorder: An individual patient data meta-analysis. Acta Psychiatrica Scandinavica, 128(3), 149–162.CrossRefGoogle ScholarPubMed
Burdick, K.E., Russo, M., Frangou, S., Mahon, K., Braga, R.J., Shanahan, M., & Malhotra, A.K. (2014). Empirical evidece for discrete neurocognitive subgroups in bipolar disorder: clinical implications. Psychological Medicine, 44(14), 3083–3096.CrossRefGoogle Scholar
Burt, T., Prudic, J., Peyser, S., Clark, J., & Sackeim, H.A. (2000). Learning and memory in bipolar and unipolar major depression: Effects of aging. Neuropsychiatry, Neuropsychology, and Behavioral Neurology, 13(4), 246–253.Google ScholarPubMed
Chalela, J.A., Alsop, D.C., Gonzalez-Atavales, J.B., Maldjian, J.A., Kasner, S.E., & Detre, J.A. (2000). Magnetic resonance perfusion imagin in acute ischemic stroke using continuous arterial spin labeling. Stroke, 31, 680–687.Google Scholar
Chen, C.-H., Suckling, J., Lennox, B., Ooi, C., & Bullmore, E.A. (2011). A quantitative meta- Analysis of fMRI studies in bipolar disorder. Bipolar Disorders, 13, 1–15.CrossRefGoogle ScholarPubMed
Coderre, E.L., & van Heuven, W.J. (2013). Modulations of the executive control network by stimulus onset asynchrony in a stroop task. BMC Neuroscience, 14, 79.Google Scholar
Cohen, H., Kaplan, Z., Kotler, M., Mittelman, I., Osher, Y., & Bersudsky, Y. (2003). Impaired heart rate variability in euthymic bipolar patients. Bipolar Disorders, 5, 138–143.Google Scholar
Corbetta, M., Meizin, F.M., Shulman, G.L., & Petersen, S.E. (1993). A PET study of visuospatial Attention. Journal of Neuroscience, 13(3), 1202–1226.Google Scholar
Cox, R.W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computational Biomedical Research, 29, 162–173.Google Scholar
Culha, A.F., Osman, O., Dogangun, Y., Filiz, K., Suna, K., Kalkan, O.N., … Beyza, A. (2008). Changes in regional cerebral blood flow demonstrated by 99mTc-HMPAO SPECT in euthymic bipolar patients. European Archives of Psychiatry and Clinical Neuroscience, 358(3), 144–151.Google Scholar
Culham, J.C., & Kanwisher, N.G. (2001). Neuroimaging of cognitive functions in human parietal cortex. Current Opinion in Neurobiology, 11(2), 157–163.Google Scholar
Dale, A.M., Fischl, B., & Sereno, M.I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage, 9, 179–194.CrossRefGoogle ScholarPubMed
D’Agostino, R.B., Wolf, P.A., Belanger, A.J., & Kannel, W.B. (1994). Stroke risk profile: Adjustment for antihypertensive medication. The Framingham Study. Stroke, 25(1), 40–43.CrossRefGoogle ScholarPubMed
Deckersbach, T., Dougherty, D.D., Savage, C., McMurrich, S., Fischmann, A.J., Nierenberg, A., … Rauch, S.L. (2006). Impaired recruitment of the dorsolateral prefrtonal cortex and hippocampus during encoding in bipolar disorder. Biological Psychiatry, 59(2), 138–146.CrossRefGoogle Scholar
Delis, D.C., Kaplan, E., & Kramer, J.H. (2001). D-KEFS examiner’s manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Desikan, R.S., Segonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., … Killiany, R.J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31, 968–980.Google Scholar
Domino, E.F., Minoshima, S., Guthrie, S., Ohl, L., Ni, L., Koeppe, R.A., & Zubieta, J.K. (2000). Nicotine effects on regional cerebral blood flow in awake, resting tobacco smokers. Synapse, 38(3), 313–321.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Eyler, L.T., Jeste, D.V., & Brown, G.G. (2008). Brain response abnormalities during verbal learning among patients with schizophrenia. Psychiatry Research, 162(1), 11–25.Google Scholar
Friedman, M.J., Culver, C.M., & Ferrell, R.B. (1977). On the safety of long-term treatment with lithium. American Journal of Psychiatry, 134(10), 1123–1126.Google Scholar
Goldstein, B.I., Kemp, D.E., Soczynska, J.K., & McIntyre, R.S. (2009). Inflammation and the Phenomenology, pathophysiology, comorbidity, and treatment of bipolar disorder: A systematic review of the literature. Journal of Clinical Psychiatry, 70(8), 1078–1090.Google Scholar
Green, M.F., Kern, R.S., & Heaton, R.K. (2004). Longitudinal studies of cognition and functional outcome in schizophrenia: Implications for MATRICS. Schizophrenia Research, 72(1), 41–51.Google Scholar
Harrow, M., Goldberg, J.F., Grossman, L.S., & Meltzer, H.Y. (1990). Outcome in manic disorders. A naturalistic follow-up study. Archives of General Psychiatry, 47(7), 665–671.Google Scholar
Hassel, S., Almeida, J.R.C., Kerr, N., Nau, S., Ladouceur, C.D., Fissell, K., … Phillips, M.L. (2008). Elevated striatal and decreased dorsolateral prefrontal cortical activity in response to emotional stimuli in euthymic bipolar disorder: No associations with psychotropic medication load. Bipolar Disorders, 10, 916–927.Google Scholar
Henry, B.L., Minassian, A., Paulus, M.P., Geyer, M.A., & Perry, W. (2009). Heart rate variability in bipolar mania and schizophrenia. Journal of Psychiatric Research, 44(3), 168–176.Google Scholar
Jespersen, S.N., & Ostergaard, L. (2012). The roles of cerebral blood flow, capillary transit time Heterogeneity, and oxygen tension in brain oxygenation and metabolism. Journal of Cerebral Blood Flow and Metabolism, 32, 264–277.Google Scholar
Jung, Y., Wong, E.C., & Liu, T.T. (2010). Multiphase pseudocontinuous arterial spin labeling (MP-PCASL) for robust quantification of cerebral blood flow. Magnetic Resonance in Medicine, 64, 799–810.Google Scholar
Kay, S.R., Fiszbein, A., & Opler, L.A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13, 261–276.Google Scholar
Kerns, J.G., Cohen, J.D., MacDonald, A.W., Cho, R.Y., Stenger, A., & Carter, C.S. (2004). Monitoring and adjustments in control. Science, 303, 1023–1026.Google Scholar
Kessler, R.C., Berglund, P., Demler, O., Jin, R., Merikangas, K.R., & Walters, E.E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey replication. The Archives General Psychiatry, 62(6), 593–602.Google Scholar
Kilbourne, A.M., Cornelius, J.R., Han, X., Pincus, H.A., Shad, M., Salloum, I., … Haas, G.L. (2004). Burden of general medical conditions among individuals with bipolar disorder. Bipolar Disorders, 6(5), 368–373.Google Scholar
Kim, M.A., Tura, E., Potkin, S.G., Fallon, J.H., Manoach, D.S., Calhoun, V.D., … Turner, J.A. (2010). Working memory circuitry in schizophrenia shows widespread cortical inefficiency and compensation. Schizophrenia Research, 117(1), 42–51.Google Scholar
Kim, S.B. (1995). Quantification of relative cerebral blood flow change by flow-sensitive alternating inversion recover (FAIR) technique: Application to functional mapping. Magnetic Resonance Medicine, 34(3), 293–301.Google Scholar
Kronhaus, D.M., Lawrence, N.S., Williams, A.M., Frangou, S., Brammer, M.J., Williams, S.C., … Phillips, M.L. (2006). Stroop performance in bipolar disorder: Further evidence for abnormalities in the ventral prefrontal cortex. Bipolar Disorders, 8(1), 28–39.CrossRefGoogle ScholarPubMed
Lee, J.S., Kim, B., Hong, Y., & Joo, Y.H. (2012). Heart rate variability in the subsyndromal depressive phase of bipolar disorder. Psychiatry and Clinical Neurosciences, 66(4), 361–366.Google Scholar
Liu, T.T., & Brown, G.G. (2007). Measurement of cerebral perfusion with arterial spin labeling: Part 1. Methods. Journal of the International Neuropsychological Society, 13, 517–525.Google Scholar
MacDonald, A.W., Cohen, J.D., Stenger, V.A., & Carter, C.S. (2000). Dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288, 1835–1838.Google Scholar
Martino, D.J., Marengo, E., Igoa, A., Scapola, M., Ais, E.D., Perinot, L., & Strejilevich, S.A. (2009). Neurocognitive and symptomatic predictors of functional outcome in bipolar disorders: A prospective 1 year follow-up study. Journal of Affective Disorders, 116(1-2), 37–42.Google Scholar
Matsumoto, K., & Tanaka, K. (2004). Conflict and control. Science, 303, 969–970.Google Scholar
McKenna, B.S., Sutherland, A.N., Legenkaya, A.P., & Eyler, L.T. (2014). Abnormalities of Brain response during encoding into verbal working memory among euthymic patients With bipolar disorder. Bipolar Disorders, 16, 289–299.CrossRefGoogle ScholarPubMed
Migliorini, M., Mendez, M.O., & Bianchi, A.M. (2012). Study of heart rate variability in bipolar disorder: Linear and non-linear parameters during sleep. Frontiers in Neuroengineering, 22(4), 1–7.Google Scholar
Milham, M.P., Banich, M.T., & Barad, V. (2003). Competition for priority in processing prefrontal cortex’s involvement in top-down control: An event-related fMRI study of the Stroop task. Brain Research, 17(2), 212–222.Google Scholar
Morriss, R., & Mohammed, F.A. (2005). Metabolism, lifestyle and bipolar affective disorder. Journal Psychopharmacology, 19(6), 94–101.CrossRefGoogle ScholarPubMed
Murray, C.J.L., & Lopez, A.D. (1994). Quantifying disability: Data, methods, and results. Bulletin of the World Health Organization, 71(3), 481–494.Google Scholar
Murray, D.P., Weiner, M., Prabhakar, M., & Fiederowicz, J.G. (2009). Mania and mortality: Why the excess cardiovascular risk in bipolar disorder? Current Psychiatry Reports, 11(6), 475–480.Google Scholar
Paulmen, R.G., Devous, M.D. Sr., Gregory, R.R., Herman, J.H., Jennings, L., Bonte, F.J., … Raese, J.D. (1990). Hypofrontality and cognitive impairment in Schizophrenia: Dynamic single-photon tomography and neuropsychological assessment of schizophrenic brain function. Biological Psychiatry, 27(4), 377–399.CrossRefGoogle Scholar
Phillips, M., Travis, M., Fagiolini, A., & Kupfer, D. (2008). Medication effects in neuroimaging Studies of bipolar disorder. American Journal of Psychiatry, 165, 313–320.CrossRefGoogle ScholarPubMed
Ragland, J.D., Gur, R.C., Glahn, D.C., Censits, D.M., Smith, R.J., Lazarev, M.G., … Gur, R.E. (1998). Frontotemporal cerebral blood flow changes during executive and Declarative memory tasks in schizophrenia: A positron emission tomography study. Neuropsychology, 12(3), 399–413.CrossRefGoogle ScholarPubMed
Richard Jennings, J., Allen, B., Gianaros, P.J., Thayer, J.F., & Manuck, S.B. (2014). Focusing neurovisceral integration: Cognition, heart rate variability, and cerebral blood flow. Psychophysiology, [E-pub ahead of print].Google Scholar
Robinson, L.J., & Ferrier, I.N. (2006). Evolution of cognitive impairment in bipolar disorder: A systematic review of cross-sectional evidence. Bipolar Disorders, 8(2), 103–116.Google Scholar
Rosa, A.R., Sanchez-Moreno, J., Martinez-Aran, A., Salamero, M., Torrent, C., Reinares, M., … Vieta, E. (2007). Validity and reliability of the Functioning Assessment Short Test (FAST) in bipolar disorder. Clinical Practice and Epidemiology in Mental Health, 7, 3–5.Google Scholar
Roth, R.M., Koven, N.S., Randolph, J.J., Flashman, L.A., Pixley, H.S., Ricketts, S.M., … Saykin, A.J. (2006). Functional magnetic resonance imaging of executive control in bipolar disorder. Neuroreport, 17(11), 1085–1089.Google Scholar
Sanchez-Moreno, J., Martinez-Aran, A., Tabares-Seisdedos, R., Torrent, C., Viete, E., & Ayuso- Mateos, J.L. (2009). Functioning and disability in bipolar disorder: An extensive review. Psychotherapy and Psychosomatics, 78(5), 285–297.CrossRefGoogle ScholarPubMed
Savard, R.J., Rey, A.C., & Post, R.M. (1980). Halstead-Reitan Category Test in bipolar and unipolar affective disorders. Relationship to age and phase of illness. The Journal of Nervous and Mental Disease, 168(5), 297–304.Google Scholar
Sodhi, S.K., Linder, J., Chenard, C.A., Miller, D.D., Haynes, W.G., & Fiederowicz, J.G. (2012). Evidence for accelerated vascular aging in bipolar disorder. Journal of Psychosomatic Research, 73, 175–179.Google Scholar
Sheehan, D.V., Lecruibier, Y., Sheehan, K.H., Amorim, P., Janavs, J., Weiller, E., … Dunbar, G.C. (1998). The mini-international neuropsychiatric interview (M.I.N.I): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59(Suppl. 20), S22–S23.Google Scholar
Shin, D.D., Ozyurt, I.B., & Liu, T.T. (2013). The cerebral blood flow biomedical informatics research network (CBFBIRN) database and analysis pipeline for arterial spin labeling MRI data. Frontiers in Neuroinformatics, 7(2), 1–17.Google Scholar
Spitzer, R.L., Williams, J.B.W., Gibbon, M., & First, M.B. (1995). Biometrics Research. Structured clinical interview for DSM-IV patient version (SCIDI/P, Version 2.0), SPSS Inc. Released 2005. SPSS for Windows, Version 14.0. Chicago: SPSS Inc.Google Scholar
Strakowski, S.M., Adler, C.M., Holland, S.K., Mills, N.P., DelBello, M.P., & Eliassen, J.C. (2005). Abnormal FMRI brain activation in euthymic bipolar Disorder during a counting STROOP interference task. American Journal of Psychiatry, 162(9), 1697–1705.Google Scholar
Takeuchi, H., Taki, Y., Hashizume, H., Sassa, Y., Nagase, T., Nouchi, R., & Kawashima, R. (2011). Cerebral blood flow during rest associates with general intelligence and creativity. PLoS One, 6(9), e25532.Google Scholar
Tohen, M., Zarate, C.A. Jr., Hennen, J., Khalsa, H.M., Strakowski, S.M., Gebre-Medhin, P., … Baldessarini, R.J. (2003). The McLean-Harvard First-Episode Mania Study: prediction of recovery and first recurrence. The American Journal of Psychiatry, 160(12), 2099–2107.Google Scholar
Trajkovic, G., Starcevic, V., Latas, M., Lestarevic, M., Ille, T., Bukumeiric, Z., & Marinkovic, J. (2011). Reliability of the Hamilton Rating Scare for Depression: A meta-analysis over a Period of 49 years. Psychiatry Research, 189, 1–9.Google Scholar
Velligan, D.I., Mahurin, R.K., Diamond, P.L., Hazleton, B.C., Eckert, S.L., & Miller, A.L. (1997). The functional significance of symptomology and cognitive function in schizophrenia. Schizophrenia Research, 25(1), 21–31.Google Scholar
Wagner, G., Sinsel, E., Sobanski, T., Kohler, S., Marinou, V., Mentzel, H.J., … Schlosser, R.G. (2006). Cortical inefficiency in patients with unipolar depression: An event related FMRI study with the Stroop task. Biological Psychiatry, 59(10), 958–965.Google Scholar
Wang, J.H., Qiu, M.L., & Constable, R.T. (2005). In vivo method for correcting transmit/receive Nonuniformities with phased array coils. Magnetic Resonance Imaging, 18, 649–655.Google Scholar
Weinberger, D.R., Berman, K.F., & Zec, R.F. (1986). Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. Archives of General Psychiatry, 43(2), 114–124.Google Scholar
Wierenga, C.E., Clark, L.R., Dev, S.I., Shin, D.D., Jurick, S.M., Rissman, R.A., … Bondi, M.W. (2013). Interaction of age and APOE genotype on cerebral blood flow at rest. Journal of Alzheimer’s Disease, 34(4), 921–935.Google Scholar
Young, R.C., Biggs, J.T., Zeigler, V.E., & Meyer, D.A. (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry, 133, 429–435.CrossRefGoogle ScholarPubMed