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Changes in regional cerebral blood flow on recovery from depression

Published online by Cambridge University Press:  09 July 2009

C. J. Bench
Affiliation:
Academic Department of Psychiatry, Royal Free Hospital School of Medicine; MRC Cyclotron Unit, Hammersmith Hospital; National Hospital for Neurology and Neurosurgery, London
R. S. J. Frackowiak
Affiliation:
Academic Department of Psychiatry, Royal Free Hospital School of Medicine; MRC Cyclotron Unit, Hammersmith Hospital; National Hospital for Neurology and Neurosurgery, London
R. J. Dolan*
Affiliation:
Academic Department of Psychiatry, Royal Free Hospital School of Medicine; MRC Cyclotron Unit, Hammersmith Hospital; National Hospital for Neurology and Neurosurgery, London
*
1Address for correspondence: Dr R. J. Dolan, National Hospital for Neurology and Neurosurgery, Queen Square, London WC1 3BG.

Synopsis

We have previously described focal abnormalities of regional cerebral blood flow (rCBF) in the left dorsolateral prefrontal cortex (DLPFC), anterior cingulate cortex and angular gyrus in 40 patients with major depression. We now report on the patterns of change in rCBF in a subgroup of 25 of the same patients who were rescanned following clinical remission of depression. Fifteen patients were scanned when optimally matched for drug treatment (4) or drug free on both occasions (11). The other 10 patients were fully recovered but could not be matched for drug status for clinical and ethical reasons. In a paired comparison of the same patients when ill and following recovery it was evident that remission was associated with a significant increase in rCBF in the left DLPFC and medial prefrontal cortex including anterior cingulate. Increases in rCBF in the angular gyrus were not seen when the comparison of depressed and recovered scans was matched for medication. The previously described relationship between clinical symptoms and brain perfusion in the depressed state was no longer present in the recovered state; this supports the hypothesis of state relatedness. Thus, recovery from depression is associated with increases in rCBF in the same areas in which focal decreases in rCBF are described in the depressed state in comparison with normal controls.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Abas, M. A., Sahakian, B. J. & Levy, R. (1990). Neuropsychological deficits and CT scan changes in elderly depressives. Psychological Medicine 20, 507520.Google Scholar
Allen, M. G. (1976). Twin studies of affective illness. Archives of General Psychiatry 33, 14761478.CrossRefGoogle ScholarPubMed
Austin, M. -P., Dougall, N., Ross, M., Murray, C., O'Carroll, R. E., Moffoot, A., Ebmeier, K. P. & Goodwin, G. M. (1992 a). Single photon emission tomography with 99mTc-exametazime in major depression and the pattern of brain activity underlying the psychotic/neurotic continuum. Journal of Affective Disorders 26, 3144.Google Scholar
Austin, M. -P., Ross, M., Murray, C., O'Carroll, R. E., Ebmeier, K. P. & Goodwin, G. M. (1992 b). Cognitive function in major depression. Journal of Affective Disorders 25, 2130.Google Scholar
Bailey, D. L., Friston, K. J., Jones, T. & Frackowiak, R. S. J. (1991). Physical validation of statistical parametric mapping. Journal of Cerebral Blood Flow and Metabolism 11 (Suppl. 2), S150.Google Scholar
Ballantine, H. T. Jr., Bouckoms, A. J., Thomas, E. K. & Giriunas, I. E. (1987). Treatment of psychiatric illness by stereotactic cingulotomy. Biological Psychiatry 22, 807819.CrossRefGoogle ScholarPubMed
Barris, R. W. & Shuman, H. R. (1953). Bilateral anterior cingulate gyrus lesions: syndrome of the anterior cingulate gyri. Neurology 3, 4452.Google Scholar
Baxter, L. R., Phelps, M. E., Mazziotta, J. C., Schwartz, J. M., Gerner, R. H., Selin, C. E. & Sumida, R. M. (1985). Cerebral metabolic rates for glucose in mood disorders. Studies with positron emission tomography and fluorodeoxyglucose F18. Archives of General Psychiatry 42, 441447.Google Scholar
Baxter, L. R., Schwartz, J. M., Phelps, M. E., Mazziotta, J. C., Guze, B. H., Selin, C. E., Gerner, R. H. & Sumida, R. M. (1989). Reduction of prefrontal cortex metabolism common to three types of depression. Archives of General Psychiatry 46, 243250.Google Scholar
Bench, C. J., Friston, K. J., Brown, R. G., Scott, L., Frackowiak, R. S. J. & Dolan, R. J. (1992). The anatomy of melancholia. Abnormalities of regional cerebral blood flow in major depression. Psychological Medicine 22, 607615.Google Scholar
Bench, C. J., Friston, K. J., Brown, R. G., Frackowiak, R. S. J. & Dolan, R. J. (1993 a). Regional cerebral blood flow in depression: the relationship with clinical syndromes. Psychological Medicine 23, 579590.CrossRefGoogle Scholar
Bench, C. J., Frith, C. D., Grasby, P. M., Friston, K. J., Paulesu, E., Frackowiak, R. S. J. & Dolan, R. J. (1993 b). Investigations of the functional anatomy of attention using the Stroop test. Neuropsychologia 31, 907922.Google Scholar
Berger, B., Gaspar, P. & Verney, C. (1991). Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends in Neuroscience 14, 2126.Google Scholar
Bertelsen, A., Harvald, B. & Hauge, M. (1977). A Danish twin study of manic depressive disorders. British Journal of Psychiatry 130, 330351.CrossRefGoogle ScholarPubMed
Brown, R. M., Crane, A. M. & Goldman, P. S. (1979). Regional distribution of monoamines in the cerebral cortex and subcortical structures of the rhesus monkey: concentrations and in vivo synthesis rates. Brain Research 168, 133150.Google Scholar
Brozowski, T. J., Brown, R. M., Rosvold, H. E. & Goldman, P. S. (1979). Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of Rhesus monkey. Science 205, 929932.CrossRefGoogle Scholar
Buchsbaum, M. S., Wu, J., DeLisi, L. E., Holcomb, H. H., Kessler, R. M., Johnson, J., King, A. C., Hazlett, E., Langston, K. & Post, R. M. (1984). Frontal cortex and basal ganglia metabolic rates assessed by positron emission tomography with [18F]2-deoxy-glucose in affective illness. Journal of Affective Disorders 10, 137152.Google Scholar
Bunney, B. S. & Chioda, L. A. (1984). Mesocortical dopamine systems: further electrophysiological and pharmacological characteristics. In Monoamine Innervation of Cerebral Cortex (ed. Descarries, L., Reader, T. R. and Jasper, H. H.), pp. 263277. Liss: New York.Google Scholar
Carney, M. W. P., Roth, M. & Garside, R. F. (1965). The diagnosis of depressive symptoms and the prediction of ECT response. British Journal of Psychiatry 111, 659674.Google Scholar
Coffey, C. E., Wilkinson, W. E., Weiner, R. D., Parashos, I. A., Djang, W. T., Webb, M. C., Figiel, G. S. & Spritzer, C. E. (1993). Quantitative cerebral anatomy in depression. Archives of General Psychiatry 50, 716.CrossRefGoogle ScholarPubMed
Cohen, R. M., Semple, W. E., Gross, M., Nordahl, T. E., King, A. C., Pickar, D. & Post, R. M. (1989). Evidence for common alterations in cerebral glucose metabolism in major affective disorders and schizophrenia. Neuropsychopharmacology 2, 241254.CrossRefGoogle ScholarPubMed
Cohen, R. M., Gross, M., Nordahl, T. E., Semple, W. E., Oren, D. A. & Rosenthal, N. (1992). Preliminary data on the metabolic brain pattern of patients with winter seasonal affective disorder. Archives of General Psychiatry 49, 545552.Google Scholar
Consensus Development Panel (1985). NIMH/NIH Consensus Development Conference Statement: mood disorders: pharmacologic prevention of recurrences. American Journal of Psychiatry 142, 469476.Google Scholar
Corbetta, M., Miezin, F. M., Dobmeyer, S., Shulman, G. L. & Petersen, S. E. (1990). Attentional modulation of neural processing of shape, color, and velocity in humans. Science 248, 15561559.CrossRefGoogle ScholarPubMed
Coryell, W. & Winokur, G. (1982). Course and outcome. In Handbook of Affective Disorders (ed. Paykel, E. S.), pp. 93106. Churchill Livingstone: Edinburgh.Google Scholar
Coryell, W., Endicott, J. & Keller, M. B. (1990). Outcome of patients with chronic affective disorder: a five-year follow-up. American Journal of Psychiatry 147, 16271633.Google ScholarPubMed
Cowen, P. J. (1991). Biological markers of depression. Psychological Medicine 21, 831836.Google Scholar
Cowen, P. J. & Anderson, I. M. (1991). 5-Hydroxytryptamine in Mental Illness: A Spectrum of Ideas, pp. 124142. Oxford University Press: Oxford.Google Scholar
Damasio, A. R. & Van Hoesen, G. W. (1983). Emotional disturbance associated with focal lesions of the limbic front lobe. In Neuropsychology of Human Emotion (ed. Heilman, K. and Satz, P.), pp. 85110. Guilford: New York.Google Scholar
De Keyser, J., Herregodts, P. & Ebinger, G. (1990). The mesoneocortical dopamine neuron system. Neurology 40, 16601662.Google Scholar
Dolan, R. J., Calloway, S. P. & Mann, A. H. (1985). Cerebral ventricular size in depressed subjects. Psychological Medicine 15, 873878.CrossRefGoogle ScholarPubMed
Dolan, R. J., Calloway, S. P., Thacker, P. & Mann, A. H. (1986). The cerebral cortical appearance in depressed subjects. Psychological Medicine 16, 775779.Google Scholar
Dolan, R. J., Bench, C. J., Liddle, P. F., Friston, K. J., Frith, C. D., Grasby, P.M. & Frackowiak, R. S. J. (1993). Dorsolateral prefrontal cortex dysfunction in the major psychoses: symptom or disease specificity? Journal of Neurology, Neurosurgery and Psychiatry 56, 12901294.Google Scholar
Dolan, R. J., Bench, C. J., Brown, R. G., Scott, L. & Frackowiak, R. S. J. (1994). Neuropsychological dysfunction in depression; the relationship to cerebral blood flow. Psychological Medicine 24, 849857.Google Scholar
Drevets, W. C. & Raichle, M. E. (1992). Neuroanatomical circuits in depression: implications for treatment mechanisms. Psychopharmacology Bulletin 28, 261274.Google ScholarPubMed
Drevets, W. C., Videen, T. O., Price, J. L., Preskorn, S. H., Carmichael, T. & Raichle, M. E. (1992). A functional anatomical study of unipolar depression. Journal of Neuroscience 12, 36283641.CrossRefGoogle ScholarPubMed
Endicott, J. & Spitzer, R. L. (1978). A diagnostic interview. The Schedule for Affective Disorders and Schizophrenia. Archives of General Psychiatry 35, 837844.Google Scholar
Fazekas, F., Alavi, A., Chawluk, J. B., Zimmerman, R. A., Hackney, D., Bilaniuk, L., Rosen, M., Alves, W. M., Hurtig, H. I., Jamieson, D. G., Kushner, M. J. & Reivich, M. (1989). Comparison of CT, MR and PET in Alzheimer's dementia and normal aging. Journal of Nuclear Medicine 30, 16071615.Google ScholarPubMed
Foltz, E. L. & White, L. E. Jr. (1962). Pain ‘Relief’ by frontal cingulotomy. Journal of Neurosurgery 19, 89100.CrossRefGoogle Scholar
Frackowiak, R. S. J., Lenzi, G. -L., Jones, T. & Heather, J. D. (1980). Quantitative measurement of regional cerebral blood flow and oxygen metabolism in man using 15O and positron emission tomography: theory, procedure, and normal values. Journal of Computer Assisted Tomography 4, 727736.Google Scholar
Frank, E., Prien, R. F., Jarrett, R. B., Keller, M. B., Kupfer, D. J., Lavori, P. W., Rush, A. J. & Weissman, M. M. (1991). Conceptualization and rationale for consensus definitions of terms in major depressive disorder. Archives of General Psychiatry 48, 851855.Google Scholar
Friston, K. J. & Frackowiak, R. S. J. (1991). Imaging functional anatomy. In Brainwork 2: Alfred Benzon Symposium, pp. 111. Munksgaard: Copenhagen.Google Scholar
Friston, K. J., Frith, C. D., Liddle, P. F., Dolan, R. J.Lammertsma, A. A. & Frackowiak, R. S. J. (1990). The relationship between global and local changes in PET scans. Journal of Cerebral Blood Flow and Metabolism 10, 458466.Google Scholar
Friston, K. J., Frith, C. D., Liddle, P. F. & Frackowiak, R. S. J. (1991 a). Comparing functional (PET) images: the assessment of significant change. Journal of Cerebral Blood Flow and Metabolism 11, 690699.Google Scholar
Friston, K. J., Frith, C. D., Liddle, P. F. & Frackowiak, R. S. J. (1991 b). Plastic transformation of PET images. Journal of Computer Assisted Tomography 15, 634639.Google Scholar
Frith, C. D., Friston, K. J., Liddle, P. F. & Frackowiak, R. S. J. (1991). Willed action and the prefrontal cortex in man: a study with PET. Proceedings of the Royal Society of London B 244, 241246.Google Scholar
Goldman-Rakic, P. S. (1988). Topography of cognition: parallel distributed networks in primate association cortex. Annual Review of Neurosciences 11, 137156.Google Scholar
Grasby, P. M., Friston, K. J., Bench, C. J., Cowen, P. J., Frith, C. D., Liddle, P. F., Frackowiak, R. S. J. & Dolan, R. J. (1993). The effect of the dopamine agonist, apomorphine on regional cerebral blood flow in normal volunteers. Psychological Medicine 23, 605612.Google Scholar
Hachinski, V. C., Iliff, L. D., Zilhka, E., Du Boulay, G. H., McAllister, V. L., Marshall, J., Ross Russell, R. W. & Symon, L. (1975). Cerebral blood flow in dementia. Archives of Neurology 32, 632637.CrossRefGoogle ScholarPubMed
Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 5662.Google Scholar
Hurwitz, T. A., Clark, C., Murphy, E., Klonoff, H., Martin, W. R. W. & Pate, B. D. (1990). Regional cerebral glucose metabolism in major depressive disorder. Canadian Journal of Psychiatry 35, 684688.Google Scholar
Jablensky, A. (1987). Prediction of the course and outcome of depression. Psychological Medicine 17, 19.CrossRefGoogle ScholarPubMed
Jenkins, I. H., Bain, P. G., Colebatch, J. G., Thompson, P. D., Findley, L. J., Frackowiak, R. S. J., Marsden, C. D. & Brooks, D. J. (1993). A positron emission tomography study of essential tremor: evidence for overactivity of cerebellar connections. Annals of Neurology 34, 8290.Google Scholar
Johanson, M., Risberg, J., Silfverskiold, P. & Gustafson, L. (1979). Regional cerebral blood flow related to acute memory disturbances following electroconvulsive therapy in depression. Acta Neurologica Scandinavica 60 (Suppl. 72), 534535.Google Scholar
Kanaya, T. & Yonekawa, M. (1990). Regional cerebral blood flow in depression. Japanese Journal of Psychiatry 44, 571576.Google Scholar
Katona, C. L. E., Theodorou, A. E. & Horton, R. W.(1987). Alpha 2-adrenoceptors in depression. Psychiatric Developments 5, 129150.Google ScholarPubMed
Keller, M. B., Shapiro, R. W., Lavori, P. W. & Wolfe, N. (1982). Relapse in major depressive disorder: analysis with the life table. Archives of General Psychiatry 39, 911915.CrossRefGoogle ScholarPubMed
Kling, A. S., Metter, E. J., Riege, W. H. & Kuhl, D. E. (1986). Comparison of PET measurement of local brain glucose metabolism and CAT measurement of brain atrophy in chronic schizophrenia and depression. American Journal of Psychiatry 143, 175180.Google Scholar
Kraepelin, E. (1921). Manic-Depressive Insanity and Paranoia. Livingstone: Edinburgh.Google Scholar
Krishnan, K. R. R., McDonald, W. M., Escalona, P. R., Doraiswamy, P. M., Na, C., Husain, M. M., Figiel, G. S., Boyko, O. B., Ellinwood, E. H. & Nemeroff, C. B. (1992). Magnetic resonance imaging of the caudate nuclei in depression. Archives of General Psychiatry 49, 553557.Google Scholar
Kupfer, D. J., Frank, E., Perel, J. M., Cornes, C., Mallinger, A. G., Thase, M. E., McEachran, A. B. & Grochocinski, V. J. (1992). Five-year outcome for maintenance therapies in recurrent depression. Archives of General Psychiatry 49, 769773.Google Scholar
Lee, A. S. & Murray, R. M. (1988). The long-term outcome of Maudsley depressives. British Journal of Psychiatry 153, 741751.Google Scholar
Liddle, P. F., Friston, K. J., Frith, C. D., Hirsch, S. R., Jones, T. & Frackowiak, R. S. J. (1992). Patterns of cerebral blood flow in schizophrenia. British Journal of Psychiatry 160, 179186.CrossRefGoogle ScholarPubMed
MacLean, P. D. (1952). Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalography and Clinical Neurophysiology 4, 407418.Google Scholar
McCulloch, J., Savaki, H. E., McCulloch, M. C., Jehle, J. & Sokoloff, L. (1982). The distribution of alterations in energy metabolism in the rat brain produced by apomorphine. Brain Research 243, 6780.Google Scholar
Maj, M., Veltro, F., Pirozzi, R., Lobrace, S. & Magliano, L. (1992). Pattern of recurrence of illness after recovery from an episode of major depression: a prospective study. American Journal of Psychiatry 149, 795800.Google ScholarPubMed
Martinot, J. L., Hardy, P., Féline, A., Huret, J. D., Mazoyer, B., Attar-Levy, D., Pappata, S. & Syrota, A. (1990). Left prefrontal glucose hypometabolism in the depressed state: a confirmation. American Journal of Psychiatry 147, 13131317.Google ScholarPubMed
Mathew, R. J., Meyer, J. S., Semchuk, K. M., Francis, D. J. & Claghorn, J. L. (1980). Cerebral blood flow in depression. Lancet i, 1308.Google Scholar
Meltzer, H. (ed.) (1987). Psychopharmacology: The Third Generation of Progress, pp. 493686. Raven Press: New York.Google Scholar
Mesulam, M. -M. (1983). The functional anatomy and hemispheric specialization for directed attention. Trends in Neuroscience 6, 384387.Google Scholar
Mesulam, M. -M., Van Hoesen, G., Pandya, D. N. & Geschwind, N. (1977). Limbic and sensory connections of the IPL in the rhesus monkey. Brain Research 136, 393414.Google Scholar
Miller, W. R. (1975). Psychological deficit in depression. Psychological Bulletin 82, 238260.CrossRefGoogle ScholarPubMed
Nielsen, J. M. & Jacobs, L. L. (1951). Bilateral lesions of the anterior cingulate gyri. Bulletin of the Los Angeles Neurological Sciences 16, 230.Google Scholar
Oldfield, R. C. (1971). The assessment and analysis of handedness; the Edinburgh inventory. Neuropsychologia 9, 97113.Google Scholar
Pandya, D. N. & Yeterian, E. H. (1985). Architecture and connections of cortical association areas. In Cerebral Cortex, vol. 4. Association and Auditory Cortices (ed. Peters, A. and Jones, E. G.), pp. 361. Plenum Press: New York.Google Scholar
Papez, J. W. (1937). A proposed mechanism of emotion. Archives of Neurology and Psychiatry 79, 217224.Google Scholar
Pardo, J. V., Pardo, P. J., Janer, K. W. & Raichle, M. E. (1990). The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proceedings of the National Academy of Sciences USA 87, 256259.CrossRefGoogle ScholarPubMed
Petersen, S. E., Fox, P. T., Posner, M. I., Mintun, M. & Raichle, M. E. (1988). Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature 331, 585589.CrossRefGoogle ScholarPubMed
Playford, E. D., Jenkins, I. H., Passingham, R. E., Nutt, J., Frackowiak, R. S. J. & Brooks, D. J. (1992). Impaired mesial frontal and putamen activation in Parkinson's disease: a PET study. Annals of Neurology 32, 151161.CrossRefGoogle Scholar
Post, R. M., DeLisi, L. E., Holcomb, H. H., Uhde, T. W., Cohen, R. & Buchsbaum, M. S. (1987). Glucose utilization in the temporal cortex of affectively ill patients: positron emission tomography. Biological Psychiatry 22, 545553.Google Scholar
Reischies, F. M., Hedde, J. -P. & Drochner, R. (1989). Clinical correlates of cerebral blood flow in depression. Psychiatry Research 29, 323326.Google Scholar
Reynolds, C. F. III. & Kupfer, D. J. (1987). Sleep research in affective illness. State of the art circa 1987. Sleep 10, 199215.Google Scholar
Rush, J. A., Cain, J. W., Raese, J., Stewart, T. S., Waller, D. A. & Debus, J. R. (1991). Neurobiological bases for psychiatric disorders. In Comprehensive Neurology (ed. Rosenberg, R. N.), pp. 555603. Raven: New York.Google Scholar
Sackeim, H. A., Prohovnik, I., Moeller, J. R., Brown, R. P., Apter, S., Prudic, J., Devanand, D. P. & Mukherjee, S. (1990). Regional cerebral blood flow in mood disorders. I. Comparison of major depressives and normal controls at rest. Archives of General Psychiatry 47, 6070.CrossRefGoogle ScholarPubMed
Saper, C. P. (1987). Diffuse cortical projection systems: anatomical organization and role in cortical function. In Handbook of Physiology. Section 1: The Nervous System, vol. 5: Higher Cortical Function (ed. Plum, F. and Mountcastle, V.), pp. 169210. Oxford University Press: New York.Google Scholar
Scatton, B., Rouquier, L., Javoy-Agid, F. & Agid, Y. (1982). Dopamine deficiency in the cerebral cortex in Parkinson's disease. Neurology 32, 10391040.Google Scholar
Silfverskiold, P. & Risberg, J. (1989). Regional cerebral blood flow in depression and mania. Archives of General Psychiatry 46, 253259.Google Scholar
Smith, G. N., Iacono, W. G., Moreau, M., Tallman, K., Beiser, M. & Flak, B. (1988). Choice of comparison group and findings of computerised tomography in schizophrenia. British Journal of Psychiatry 153, 667674.Google Scholar
Spinks, T. J., Jones, T., Gilardi, M. C. & Heather, J. D. (1988). Physical performance of the latest generation of commercial positron scanner. IEEE Transactions on Nuclear Science 35, 721725.Google Scholar
Spitzer, R. L., Endicott, J. & Robins, E. (1977). Research Diagnostic Criteria for a Selected Group of Functional Disorders. Biometrics Research Division, New York State Psychiatric Institute: New York.Google Scholar
Talairach, J. & Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain, pp. 1122. Georg Thieme Verlag: Stuttgart.Google Scholar
Talbot, J. D., Marrett, S., Evans, A. C., Meyer, E., Bushnell, M. C. & Duncan, G. H. (1991). Multiple representations of pain in human cerebral cortex. Science 251, 13551358.Google Scholar
Uytedenhoef, P., Portelange, P., Jacquy, J., Charles, G., Linkowski, P. & Mendlewicz, J. (1983). Regional cerebral blood flow and lateralised hemispheric dysfunction in depression. British Journal of Psychiatry 143, 128132.Google Scholar
Wood, A. J., Smith, C. E., Clarke, E. E., Cowen, P. J., Aronson, J. K. & Grahame-Smith, D. G. (1991). Altered in vitro adaptive responses of lymphocyte Na+, K+-ATPase in patients with manic depressive psychosis. Journal of Affective Disorders 21, 199206.CrossRefGoogle ScholarPubMed
Woods, R. P., Cherry, S. R. & Mazziotta, J. C. (1992). A rapid automated algorithm for accurately aligning and reslicing positron emission tomography images. Journal of Computer Assisted Tomography 16, 620633.Google Scholar
Wu, J. C., Gillin, J. C., Buchsbaum, M. S., Hershey, T., Johnson, J. C. & Bunney, W. E. (1992). Effect of sleep deprivation on brain metabolism of depressed patients. American Journal of Psychiatry 149, 538543.Google ScholarPubMed