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Altered prefrontal lobe oxygenation in bipolar disorder: a study by near-infrared spectroscopy

Published online by Cambridge University Press:  24 September 2008

Y. Kubota ,
M. Toichi ,
M. Shimizu ,
R. A. Mason ,
R. L. Findling ,
K. Yamamoto ,
T. Hayashi  and
J. R. Calabrese
Y. Kubota*
Affiliation:
Health and Medical Service Center, Shiga University, Shiga, Japan Mood Disorders Program, Department of Psychiatry, Case Western Reserve University/University Hospitals Case Medical Center, Cleveland, OH, USA
M. Toichi
Affiliation:
Graduate School of Health Science, Kyoto University, Kyoto, Japan Division of Child and Adolescent Psychiatry, Case Western Reserve University/University Hospitals Case Medical Center, Cleveland, OH, USA
M. Shimizu
Affiliation:
Center for Student Health, Kobe University, Kobe, Japan
R. A. Mason
Affiliation:
Mood Disorders Program, Department of Psychiatry, Case Western Reserve University/University Hospitals Case Medical Center, Cleveland, OH, USA
R. L. Findling
Affiliation:
Division of Child and Adolescent Psychiatry, Case Western Reserve University/University Hospitals Case Medical Center, Cleveland, OH, USA
K. Yamamoto
Affiliation:
Health and Medical Service Center, Shiga University, Shiga, Japan
T. Hayashi
Affiliation:
Department of Psychiatry, Kyoto University, Kyoto, Japan
J. R. Calabrese
Affiliation:
Mood Disorders Program, Department of Psychiatry, Case Western Reserve University/University Hospitals Case Medical Center, Cleveland, OH, USA
*
*Address for correspondence: Y. Kubota, Associate Professor, M.D., Ph.D., Health and Medical Services Center, Shiga University, 1-1-1 Baba, Hikone, 522-8522Japan. (Email: [email protected])
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Abstract

Background

Previous studies have reported prefrontal cortex (PFC) pathophysiology in bipolar disorder.

Method

We examined the hemodynamics of the PFC during resting and cognitive tasks in 29 patients with bipolar disorder and 27 healthy controls, matched for age, verbal abilities and education. The cognitive test battery consisted of letter and category fluency (LF and CF), Sets A and B of the Raven's Colored Progressive Matrices (RCPM-A and RCPM-B) and the letter cancellation test (LCT). The tissue oxygenation index (TOI), the ratio of oxygenated hemoglobin (HbO2) concentration to total hemoglobin concentration, was measured in the bilateral PFC by spatially resolved near-infrared spectroscopy. Changes in HbO2 concentration were also measured.

Results

The bipolar group showed slight but significant impairment in performance for the non-verbal tasks (RCPM-A, RCPM-B and LCT), with no significant between-group differences for the two verbal tasks (LF and CF). A group×task×hemisphere analysis of variance (ANOVA) on the TOI revealed an abnormal pattern of prefrontal oxygenation across different types of cognitive processing in the bipolar group. Post hoc analyses following a group×task×hemisphere ANOVA on HbO2 concentration revealed that the bipolar group showed a greater increase in HbO2 concentration in the LCT and in RCPM-B, relative to controls.

Conclusions

Both indices of cortical activation (TOI and HbO2 concentration) indicated a discrepancy in the PFC function between verbal versus non-verbal processing, indicating task-specific abnormalities in the hemodynamic control of the PFC in bipolar disorder.

Keywords

Bipolar disordernear-infrared spectroscopyprefrontal cortextissue hemoglobin saturation
Type
Original Articles
Information
Psychological Medicine , Volume 39 , Issue 8 , August 2009 , pp. 1265 - 1275
Copyright
Copyright © 2008 Cambridge University Press

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References

Adler, CM, Holland, SK, Schmithorst, V, Tuchfarber, MJ, Strakowski, SM (2004). Changes in neuronal activation in patients with bipolar disorder during performance of a working memory task. Bipolar Disorders 6, 540–549.CrossRefGoogle ScholarPubMed
Al-Rawi, PG, Kirkpatrick, PJ (2006). Tissue oxygen index: thresholds for cerebral ischemia using near-infrared spectroscopy. Stroke 37, 2720–2725.CrossRefGoogle ScholarPubMed
Audenaert, K, Brans, B, Van Laere, K, Lahorte, P, Versijpt, J, van Heeringen, K, Dierckx, R (2000). Verbal fluency as a prefrontal activation probe: a validation study using 99mTc-ECD brain SPET. European Journal of Nuclear Medicine 27, 1800–1808.CrossRefGoogle ScholarPubMed
Bell, EC, Willson, MC, Wilman, AH, Dave, S, Silverstone, PH (2005). Differential effects of chronic lithium and valproate on brain activation in healthy volunteers. Human Psychopharmacology 20, 415–424.CrossRefGoogle ScholarPubMed
Blumberg, HP, Leung, HC, 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, 601–609.CrossRefGoogle ScholarPubMed
Cope, M, Delpy, DT (1988). System for long-term measurement of cerebral blood and tissue oxygenation on new born infants by near infra-red transillumination. Medical and Biological Engineering and Computing 26, 289–294.CrossRefGoogle Scholar
Curtis, VA, Bullmore, ET, Brammer, MJ, Wright, IC, Williams, SC, Morris, RG, Sharma, TS, Murray, RM, McGuire, PK (1998). Attenuated frontal activation during a verbal fluency task in patients with schizophrenia. American Journal of Psychiatry 155, 1056–1063.CrossRefGoogle ScholarPubMed
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
Dager, SR, Friedman, SD, Parow, A, Demopulos, C, Stoll, AL, Lyoo, IK, Dunner, DL, Renshaw, PF (2004). Brain metabolic alterations in medication-free patients with bipolar disorder. Archives of General Psychiatry 61, 450–458.CrossRefGoogle ScholarPubMed
Duncan, A, Meek, JH, Clemence, M, Elwell, CE, Tyszczuk, L, Cope, M, Delpy, DT (1995). Optical pathlength measurements on adult head, calf and forearm and the head of the newborn infant using phase resolved optical spectroscopy. Physics in Medicine and Biology 40, 295–304.CrossRefGoogle ScholarPubMed
Endicott, J, Spitzer, RL, Fleiss, JL, Cohen, J (1976). The global assessment scale. A procedure for measuring overall severity of psychiatric disturbance. Archives of General Psychiatry 33, 766–771.CrossRefGoogle Scholar
Esposito, G, Kirkby, BS, Van Horn, JD, Ellmore, TM, Berman, KF (1999). Context-dependent, neural system-specific neurophysiological concomitants of ageing: mapping PET correlates during cognitive activation. Brain 122, 963–979.CrossRefGoogle ScholarPubMed
Fallgatter, A, Strik, W (1997). Right frontal activation during the continuous performance test assessed with near-infrared spectroscopy in healthy subjects. Neuroscience Letters 223, 89–92.CrossRefGoogle ScholarPubMed
Fallgatter, AJ, Strik, WK (1998). Frontal brain activation during the Wisconsin Card Sorting Test assessed with two-channel near-infrared spectroscopy. European Archives of Psychiatry and Clinical Neuroscience 248, 245–249.CrossRefGoogle ScholarPubMed
First, M, Spitzer, R, Gibbon, M, Williams, JB (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
Gratton, G, Maier, J, Fabinai, M, Mantulin, W, Gratton, E (1994). Feasibility of intracranial near-infrared optical scanning. Psychophysiology 31, 211–215.CrossRefGoogle ScholarPubMed
Herrmann, MJ, Ehlis, AC, Fallgatter, AJ (2004). Bilaterally reduced frontal activation during a verbal fluency task in depressed patients as measured by near-infrared spectroscopy. Journal of Neuropsychiatry and Clinical Neurosciences 16, 170–175.CrossRefGoogle ScholarPubMed
Jobsis, FF (1977). Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science 198, 1264–1267.CrossRefGoogle ScholarPubMed
Kameyama, M, Fukuda, M, Yamagishi, Y, Sato, T, Uehara, T, Ito, M, Suto, T, Mikuni, M (2006). Frontal lobe function in bipolar disorder: a multichannel near-infrared spectroscopy study. Neuroimage 29, 172–184.CrossRefGoogle ScholarPubMed
Kato, T, Kato, N (2000). Mitochondrial dysfunction in bipolar disorder. Bipolar Disorders 2, 180–190.CrossRefGoogle ScholarPubMed
Kato, T, Takahashi, S, Shioiri, T, Inubushi, T (1993). Alterations in brain phosphorous metabolism in bipolar disorder detected by in vivo 31P and 7Li magnetic resonance spectroscopy. Journal of Affective Disorders 27, 53–59.CrossRefGoogle ScholarPubMed
Konradi, C, Eaton, M, MacDonald, ML, Walsh, J, Benes, FM, Heckers, S (2004). Molecular evidence for mitochondrial dysfunction in bipolar disorder. Archives of General Psychiatry 61, 300–308.CrossRefGoogle ScholarPubMed
Krakow, K, Ries, S, Daffertshofer, M, Hennerici, M (2000). Simultaneous assessment of brain tissue oxygenation and cerebral perfusion during orthostatic stress. European Neurology 43, 39–46.CrossRefGoogle ScholarPubMed
Kubota, Y, Toichi, M, Shimizu, M, Mason, RA, Coconcea, CM, Findling, RL, Yamamoto, K, Calabrese, JR (2005). Prefrontal activation during verbal fluency tests in schizophrenia – a near-infrared spectroscopy (NIRS) study. Schizophrenia Research 77, 65–73.CrossRefGoogle ScholarPubMed
Kubota, Y, Toichi, M, Shimizu, M, Mason, RA, Findling, RL, Yamamoto, K, Calabrese, JR (2006). Prefrontal hemodynamic activity predicts false memory – a near-infrared spectroscopy study. Neuroimage 31, 1783–1789.CrossRefGoogle ScholarPubMed
Kuroda, S, Houkin, K, Abe, H, Hoshi, Y, Tamura, M (1996). Near-infrared monitoring of cerebral oxygenation state during carotid endarterectomy. Surgical Neurology 45, 450–458.CrossRefGoogle ScholarPubMed
Lee, J, Folley, BS, Gore, J, Park, S (2008). Origins of spatial working memory deficits in schizophrenia: an event-related FMRI and near-infrared spectroscopy study. PLoS ONE 3, e1760.CrossRefGoogle ScholarPubMed
Lopez-Larson, MP, DelBello, MP, Zimmerman, ME, Schwiers, ML, Strakowski, SM (2002). Regional prefrontal gray and white matter abnormalities in bipolar disorder. Biological Psychiatry 52, 93–100.CrossRefGoogle ScholarPubMed
Matcher, SJ, Elwell, CE, Cooper, CE, Cope, M, Delpy, DT (1995). Absolute quantification methods in tissue near infrared spectroscopy. Proceedings of SPIE 2839, 486–495.CrossRefGoogle Scholar
Matsuo, K, Kato, N, Kato, T (2002). Decreased cerebral haemodynamic response to cognitive and physiological tasks in mood disorders as shown by near-infrared spectroscopy. Psychological Medicine 32, 1029–1037.CrossRefGoogle ScholarPubMed
Matsuo, K, Watanabe, A, Onodera, Y, Kato, N, Kato, T (2004). Prefrontal hemodynamic response to verbal-fluency task and hyperventilation in bipolar disorder measured by multi-channel near-infrared spectroscopy. Journal of Affective Disorders 82, 85–92.CrossRefGoogle ScholarPubMed
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, 550–564.CrossRefGoogle ScholarPubMed
Montgomery, SA, Asberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382–389.CrossRefGoogle ScholarPubMed
Mummery, CJ, Patterson, K, Hodges, JR, Wise, RJ (1996). Generating ‘tiger’ as an animal name or a word beginning with T: differences in brain activation. Proceedings of the Royal Society of London. Series B, Biological Sciences 263, 989–995.Google ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Pearlson, GD, Barta, PE, Powers, RE, Menon, RR, Richards, SS, Aylward, EH, Federman, EB, Chase, GA, Petty, RG, Tien, AY (1997). Ziskind-Somerfeld Research Award 1996. Medial and superior temporal gyral volumes and cerebral asymmetry in schizophrenia versus bipolar disorder. Biological Psychiatry 41, 1–14.CrossRefGoogle ScholarPubMed
Rajkowska, G, Halaris, A, Selemon, L (2001). Reductions in neuronal and glial density characterize the dorsolateral prefrontal cortex in bipolar disorder. Biological Psychiatry 49, 741–752.CrossRefGoogle ScholarPubMed
Raven, J (1962). Coloured Progressive Matrices: Sets A, AB, B. H. K. Lewis: London.Google Scholar
Sakatani, K, Katayama, Y, Yamamoto, T, Suzuki, S (1999). Changes in cerebral blood oxygenation of the frontal lobe induced by direct electrical stimulation of thalamus and globus pallidus: a near infrared spectroscopy study. Journal of Neurology, Neurosurgery and Psychiatry 67, 769–773.CrossRefGoogle ScholarPubMed
Sassi, RB, Stanley, JA, Axelson, D, Brambilla, P, Nicoletti, MA, Keshavan, MS, Ramos, RT, Ryan, N, Birmaher, B, Soares, JC (2005). Reduced NAA levels in the dorsolateral prefrontal cortex of young bipolar patients. American Journal of Psychiatry 162, 2109–2115.CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (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), 22–57.Google ScholarPubMed
Silverstone, PH, Bell, EC, Willson, MC, Dave, S, Wilman, AH (2005). Lithium alters brain activation in bipolar disorder in a task- and state-dependent manner: an fMRI study. Annals of General Psychiatry 4, 14.CrossRefGoogle Scholar
Strakowski, SM, Adler, CM, Holland, SK, Mills, N, DelBello, MP (2004). A preliminary FMRI study of sustained attention in euthymic, unmedicated bipolar disorder. Neuropsychopharmacology 29, 1734–1740.CrossRefGoogle ScholarPubMed
Sun, X, Wang, JF, Tseng, M, Young, LT (2006). Downregulation in components of the mitochondrial electron transport chain in the postmortem frontal cortex of subjects with bipolar disorder. Journal of Psychiatry and Neuroscience 31, 189–196.Google ScholarPubMed
Toichi, M, Findling, RL, Kubota, Y, Calabrese, JR, Wiznitzer, M, McNamara, NK, Yamamoto, K (2004). Hemodynamic differences in the activation of the prefrontal cortex: attention vs. higher cognitive processing. Neuropsychologia 42, 698–706.CrossRefGoogle ScholarPubMed
van der Zee, P, Cope, M, Arridge, SR, Essenpreis, M, Potter, LA, Edwards, AD, Wyatt, JS, McCormick, DC, Roth, SC, Reynolds, EOR, Delpy, DT (1992). Experimentally measured optical pathlengths for the adult head, calf and forearm and the head of the newborn infant as a function of inter optode spacing. Advances in Experimental Medicine and Biology 316, 143–153.CrossRefGoogle ScholarPubMed
Villringer, A, Planck, J, Hock, C, Schleinkofer, L, Dirnagl, U (1993). Near infrared spectroscopy (NIRS): a new tool to study hemodynamic changes during activation of brain function in human adults. Neuroscience Letters 154, 101–104.CrossRefGoogle ScholarPubMed
Wechsler, D (1981). Wechsler Adult Intelligence Scale – Revised. Psychological Corporation: New York.Google Scholar
Young, RC, Biggs, JT, Zeigler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429–435.CrossRefGoogle ScholarPubMed