Increased hippocampal blood volume and normal blood flow in schizophrenia

Psychiatry Research - Neuroimaging

Volumn 232, Issue 3, 2015, Pages 219-225

  Talati, Pratik ^a   Rane, Swati ^b   Skinner, Jack ^b   Gore, John ^b   Heckers, Stephan ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

CBF; CBV; DSC MRI; Dynamic susceptibility contrast; Gadolinium; Mean transit time

Indexed keywords

GADOLINIUM PENTETATE MEGLUMINE;

ADULT; ANGIOGENESIS; ARTICLE; BRAIN BLOOD FLOW; BRAIN BLOOD VOLUME; BRAIN PERFUSION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HEMODYNAMIC PARAMETERS; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MALE; MEAN TRANSIT TIME; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; SCHIZOPHRENIA; BLOOD VOLUME; BRAIN CIRCULATION; HEMODYNAMICS; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; PROCEDURES; VASCULARIZATION; YOUNG ADULT;

ADULT; BLOOD VOLUME; CEREBROVASCULAR CIRCULATION; FEMALE; HEMODYNAMICS; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84929514877     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2015.03.007     Document Type: Article

References (79)

1. Bellani M., Peruzzo D., Isola M., Rambaldelli G., Perlini C., Baiano M., Cerini R., Andreone N., Barillari M., Mucelli R.P., Balestrieri M., Tansella M., Bertoldo A., Brambilla P. Cerebellar and lobar blood flow in schizophrenia: a perfusion weighted imaging study. Psychiatry Research: Neuroimaging 2011, 193:46-52.
2. Ben Bashat D., Artzi M., Ben Ami H., Aizenstein O., Blumenthal D.T., Bokstein F., Corn B.W., Ram Z., Kanner A.A., Lifschitz-Mercer B., Solar I., Kolatt T., Palmon M., Edrei Y., Abramovitch R. Hemodynamic response imaging: a potential tool for the assessment of angiogenesis in brain tumors. PloS One 2012, 7:e49416.
3. Benes F.M., Kwok E.W., Vincent S.L., Todtenkopf M.S. A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biological Psychiatry 1998, 44:88-97.
4. Boxerman J.L., Hamberg L.M., Rosen B.R., Weisskoff R.M. MR contrast due to intravascular magnetic susceptibility perturbations. Magnetic Resonance in Medicine 1995, 34:555-566.
5. Brambilla P., Cerini R., Fabene P.F., Andreone N., Rambaldelli G., Farace P., Versace A., Perlini C., Pelizza L., Gasparini A., Gatti R., Bellani M., Dusi N., Barbui C., Nose M., Tournikioti K., Sbarbati A., Tansella M. Assessment of cerebral blood volume in schizophrenia: a magnetic resonance imaging study. Journal of Psychiatric Research 2007, 41:502-510.
6. Buchsbaum M.S., Haier R.J., Potkin S.G., Nuechterlein K., Bracha H.S., Katz M., Lohr J., Wu J., Lottenberg S., Jerabek P.A., Trenary M., Tafalla R., Reynolds C., Bunney W.E. Frontostriatal disorder of cerebral metabolism in never-medicated schizophrenics. Archives of General Psychiatry 1992, 49:935-942.
7. Calamante F., Gadian D.G., Connelly A. Quantification of perfusion using bolus tracking magnetic resonance imaging in stroke: assumptions, limitations, and potential implications for clinical use. Stroke 2002, 33:1146-1151.
8. Chan K.H., Miller J.D., Dearden N.M., Andrews P.J., Midgley S. The effect of changes in cerebral perfusion pressure upon middle cerebral artery blood flow velocity and jugular bulb venous oxygen saturation after severe brain injury. Journal of Neurosurgery 1992, 77:55-61.
9. Choi Y.J., Kim H.S., Jahng G.H., Kim S.J., Suh D.C. Pseudoprogression in patients with glioblastoma: added value of arterial spin labeling to dynamic susceptibility contrast perfusion MR imaging. Acta Radiologica 2013, 54:448-454.
10. Cohen B.M., Yurgelun-Todd D., English C.D., Renshaw P.F. Abnormalities of regional distribution of cerebral vasculature in schizophrenia detected by dynamic susceptibility contrast MRI. The American Journal of Psychiatry 1995, 152:1801-1803.
11. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research 1996, 29:162-173.
12. Donahue M.J., Faraco C.C., Strother M.K., Chappell M.A., Rane S., Dethrage L.M., Hendrikse J., Siero J.C. Bolus arrival time and cerebral blood flow responses to hypercarbia. Journal of Cerebral Blood Flow and Metabolism 2014, 34:1243-1252.
13. Ertugrul A., Volkan-Salanci B., Basar K., Karli Oguz K., Demir B., Ergun E.L., Senturk S., Erbas B., Cila A., Ulug B. The effect of clozapine on regional cerebral blood flow and brain metabolite ratios in schizophrenia: relationship with treatment response. Psychiatry Research: Neuroimaging 2009, 174:121-129.
14. Fabene P.F., Farace P., Brambilla P., Andreone N., Cerini R., Pelizza L., Versace A., Rambaldelli G., Birbaumer N., Tansella M., Sbarbati A. Three-dimensional MRI perfusion maps: a step beyond volumetric analysis in mental disorders. Journal of Anatomy 2007, 210:122-128.
15. First M.B., Spitzer Robert L., Miriam Gibbon, Williams Janet B.W. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition With Psychotic Screen (SCID-I/P W/ PSY SCREEN) 2002, Biometrics Research, New York State Psychiatric Institute, New York, NY.
16. Friston K.J., Liddle P.F., Frith C.D., Hirsch S.R., Frackowiak R.S. The left medial temporal region and schizophrenia. A PET study. Brain 1992, 115(Pt 2):367-382.
17. Gardner D.M., Murphy A.L., O'Donnell H., Centorrino F., Baldessarini R.J. International consensus study of antipsychotic dosing. The American Journal of Psychiatry 2010, 167:686-693.
18. Gevers S., van Osch M.J., Bokkers R.P., Kies D.A., Teeuwisse W.M., Majoie C.B., Hendrikse J., Nederveen A.J. Intra- and multicenter reproducibility of pulsed, continuous and pseudo-continuous arterial spin labeling methods for measuring cerebral perfusion. Journal of Cerebral Blood Flow and Metabolism 2011, 31:1706-1715.
19. Grubb R.L., Raichle M.E., Eichling J.O., Ter-Pogossian M.M. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 1974, 5:630-639.
20. Heckers S., Konradi C. Hippocampal pathology in schizophrenia. Current Topics in Behavioral Neurosciences 2010, 4:529-553.
21. Heckers, S., Konradi, C., 2014. GABAergic mechanisms of hippocampal hyperactivity in schizophrenia. Schizophrenia Research, . http://dx.doi.org/10.1016/j.schres.2014.09.041.
22. Heckers S., Rauch S.L., Goff D., Savage C.R., Schacter D.L., Fischman A.J., Alpert N.M. Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nature Neuroscience 1998, 1:318-323.
23. Heilbrun M.P., Jorgensen P.B., Boysen G. Relationships between cerebral perfusion pressure and regional cerebral blood flow in patients with severe neurological disorders. Stroke 1972, 3:181-195.
24. Homan P., Kindler J., Hauf M., Hubl D., Dierks T. Cerebral blood flow identifies responders to transcranial magnetic stimulation in auditory verbal hallucinations. Translational Psychiatry 2012, 2:e189.
25. Horn H., Federspiel A., Wirth M., Muller T.J., Wiest R., Wang J.J., Strik W. Structural and metabolic changes in language areas linked to formal thought disorder. The British Journal of Psychiatry 2009, 194:130-138.
26. Huang Y.P., Okudera T. Arterial supply to the hippocampal formation. Neuroimaging Clinics of North America 1997, 7:31-50.
27. Jiang J., Zhao L., Zhang Y., Zhang S., Yao Y., Qin Y., Wang C.Y., Zhu W. Comparative analysis of arterial spin labeling and dynamic susceptibility contrast perfusion imaging for quantitative perfusion measurements of brain tumors. International Journal of Clinical and Experimental Pathology 2014, 7:2790-2799.
28. Kawasaki Y., Suzuki M., Maeda Y., Urata K., Yamaguchi N., Matsuda H., Hisada K., Takashima T. Regional cerebral blood flow in patients with schizophrenia. A preliminary report. European Archives of Psychiatry and Clinical Neuroscience 1992, 241:195-200.
29. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 1987, 13:261-276.
30. Kindler J., Jann K., Homan P., Hauf M., Walther S., Strik W., Dierks T., Hubl D. Static and dynamic characteristics of cerebral blood flow during the resting state in schizophrenia. Schizophrenia Bulletin 2015, 41(1):163-170.
31. Konradi C., Yang C.K., Zimmerman E.I., Lohmann K.M., Gresch P., Pantazopoulos H., Berretta S., Heckers S. Hippocampal interneurons are abnormal in schizophrenia. Schizophrenia Research 2011, 131:165-173.
32. Lahti A.C., Holcomb H.H., Weiler M.A., Medoff D.R., Tamminga C.A. Functional effects of antipsychotic drugs: comparing clozapine with haloperidol. Biological Psychiatry 2003, 53:601-608.
33. Lahti A.C., Weiler M.A., Holcomb H.H., Tamminga C.A., Carpenter W.T., McMahon R. Correlations between rCBF and symptoms in two independent cohorts of drug-free patients with schizophrenia. Neuropsychopharmacology 2006, 31:221-230.
34. Li X., Sarkar S.N., Purdy D.E., Spence J.S., Haley R.W., Briggs R.W. Anteroposterior perfusion heterogeneity in human hippocampus measured by arterial spin labeling MRI. NMR in Biomedicine 2013, 26:613-621.
35. Liddle P.F., Friston K.J., Frith C.D., Frackowiak R.S. Cerebral blood flow and mental processes in schizophrenia. Journal of the Royal Society of Medicine 1992, 85:224-227.
36. Lisman J.E., Coyle J.T., Green R.W., Javitt D.C., Benes F.M., Heckers S., Grace A.A. Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends in Neurosciences 2008, 31:234-242.
37. Loeber R.T., Sherwood A.R., Renshaw P.F., Cohen B.M., Yurgelun-Todd D.A. Differences in cerebellar blood volume in schizophrenia and bipolar disorder. Schizophrenia Research 1999, 37:81-89.
38. Malaspina D., Harkavy-Friedman J., Corcoran C., Mujica-Parodi L., Printz D., Gorman J.M., Van Heertum R. Resting neural activity distinguishes subgroups of schizophrenia patients. Biological Psychiatry 2004, 56:931-937.
39. Medoff D.R., Holcomb H.H., Lahti A.C., Tamminga C.A. Probing the human hippocampus using rCBF: contrasts in schizophrenia. Hippocampus 2001, 11:543-550.
40. Miller D.D., Andreasen N.C., O'Leary D.S., Rezai K., Watkins G.L., Ponto L.L., Hichwa R.D. Effect of antipsychotics on regional cerebral blood flow measured with positron emission tomography. Neuropsychopharmacology 1997, 17:230-240.
41. Moreno H., Wu W.E., Lee T., Brickman A., Mayeux R., Brown T.R., Small S.A. Imaging the Abeta-related neurotoxicity of Alzheimer disease. Archives of Neurology 2007, 64:1467-1477.
42. Mu Q., Johnson K., Morgan P.S., Grenesko E.L., Molnar C.E., Anderson B., Nahas Z., Kozel F.A., Kose S., Knable M., Fernandes P., Nichols D.E., Mailman R.B., George M.S. A single 20mg dose of the full D1 dopamine agonist dihydrexidine (DAR-0100) increases prefrontal perfusion in schizophrenia. Schizophrenia Research 2007, 94:332-341.
43. Nael K., Meshksar A., Liebeskind D.S., Wang D.J., Ellingson B.M., Salamon N., Villablanca J.P. Periprocedural arterial spin labeling and dynamic susceptibility contrast perfusion in detection of cerebral blood flow in patients with acute ischemic syndrome. Stroke 2013, 44:664-670.
44. Nordahl T.E., Kusubov N., Carter C., Salamat S., Cummings A.M., O'Shora-Celaya L., Eberling J., Robertson L., Huesman R.H., Jagust W., Budinger T.F. Temporal lobe metabolic differences in medication-free outpatients with schizophrenia via the PET-600. Neuropsychopharmacology 1996, 15:541-554.
45. Novak B., Milcinski M., Grmek M., Kocmur M. Early effects of treatment on regional cerebral blood flow in first episode schizophrenia patients evaluated with 99Tc-ECD-SPECT. Neuroendocrinology Letters 2005, 26:685-689.
46. Olney J.W., Newcomer J.W., Farber N.B. NMDA receptor hypofunction model of schizophrenia. Journal of Psychiatric Research 1999, 33:523-533.
47. Ostergaard L. Cerebral perfusion imaging by bolus tracking. Topics in Magnetic Resonance Imaging 2004, 15:3-9.
48. Ostergaard L., Sorensen A.G., Kwong K.K., Weisskoff R.M., Gyldensted C., Rosen B.R. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part II: experimental comparison and preliminary results. Magnetic Resonance in Medicine 1996, 36:726-736.
49. Ostergaard L., Weisskoff R.M., Chesler D.A., Gyldensted C., Rosen B.R. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: mathematical approach and statistical analysis. Magnetic Resonance in Medicine 1996, 36:715-725.
50. Ota M., Ishikawa M., Sato N., Okazaki M., Maikusa N., Hori H., Hattori K., Teraishi T., Ito K., Kunugi H. Pseudo-continuous arterial spin labeling MRI study of schizophrenic patients. Schizophrenia Research 2014, 154:113-118.
51. Parkes L.M., Rashid W., Chard D.T., Tofts P.S. Normal cerebral perfusion measurements using arterial spin labeling: reproducibility, stability, and age and gender effects. Magnetic Resonance in Medicine 2004, 51:736-743.
52. Perkio J., Aronen H.J., Kangasmaki A., Liu Y., Karonen J., Savolainen S., Ostergaard L. Evaluation of four postprocessing methods for determination of cerebral blood volume and mean transit time by dynamic susceptibility contrast imaging. Magnetic Resonance in Medicine 2002, 47:973-981.
53. Peruzzo D., Rambaldelli G., Bertoldo A., Bellani M., Cerini R., Silvia M., Pozzi Mucelli R., Tansella M., Brambilla P. The impact of schizophrenia on frontal perfusion parameters: a DSC-MRI study. Journal of Neural Transmission 2011, 118:563-570.
54. Petersen E.T., Mouridsen K., Golay X. The QUASAR reproducibility study, Part II: results from a multi-center arterial spin labeling test-retest study. NeuroImage 2010, 49:104-113.
55. Pinkham A., Loughead J., Ruparel K., Wu W.C., Overton E., Gur R. Resting quantitative cerebral blood flow in schizophrenia measured by pulsed arterial spin labeling perfusion MRI. Psychiatry Research: Neuroimaging 2011, 194:64-72.
56. Renshaw P.F., Levin J.M., Kaufman M.J., Ross M.H., Lewis R.F., Harris G.J. Dynamic susceptibility contrast magnetic resonance imaging in neuropsychiatry: present utility and future promise. European Radiology 1997, 7(Suppl. 5):S216-S221.
57. Scheef L., Manka C., Daamen M., Kuhn K.U., Maier W., Schild H.H., Jessen F. Resting-state perfusion in nonmedicated schizophrenic patients: a continuous arterial spin-labeling 3.0-T MR study. Radiology 2010, 256:253-260.
58. Schobel S.A., Chaudhury N.H., Khan U.A., Paniagua B., Styner M.A., Asllani I., Inbar B.P., Corcoran C.M., Lieberman J.A., Moore H., Small S.A. Imaging patients with psychosis and a mouse model establishes a spreading pattern of hippocampal dysfunction and implicates glutamate as a driver. Neuron 2013, 78:81-93.
59. Schobel S.A., Lewandowski N.M., Corcoran C.M., Moore H., Brown T., Malaspina D., Small S.A. Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders. Archives of General Psychiatry 2009, 66:938-946.
60. Simonsen C.Z., Ostergaard L., Vestergaard-Poulsen P., Rohl L., Bjornerud A., Gyldensted C. CBF and CBV measurements by USPIO bolus tracking: reproducibility and comparison with Gd-based values. Journal of Magnetic Resonance Imaging 1999, 9:342-347.
61. Small S.A., Schobel S.A., Buxton R.B., Witter M.P., Barnes C.A. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nature Reviews: Neuroscience 2011, 12:585-601.
62. Swain R.A., Harris A.B., Wiener E.C., Dutka M.V., Morris H.D., Theien B.E., Konda S., Engberg K., Lauterbur P.C., Greenough W.T. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003, 117:1037-1046.
63. Talati P., Rane S., Kose S., Blackford J.U., Gore J., Donahue M.J., Heckers S. Increased hippocampal CA1 cerebral blood volume in schizophrenia. NeuroImage: Clinical 2014, 5:359-364.
64. Talati P., Rane S., Kose S., Gore J., Heckers S. Anterior-Posterior cerebral blood volume gradient in human subiculum. Hippocampus 2014, 24:503-509.
65. Tamminga C.A., Thaker G.K., Buchanan R., Kirkpatrick B., Alphs L.D., Chase T.N., Carpenter W.T. Limbic system abnormalities identified in schizophrenia using positron emission tomography with fluorodeoxyglucose and neocortical alterations with deficit syndrome. Archives of General Psychiatry 1992, 49:522-530.
66. Tanaka Y., Nagaoka T., Nair G., Ohno K., Duong T.Q. Arterial spin labeling and dynamic susceptibility contrast CBF MRI in postischemic hyperperfusion, hypercapnia, and after mannitol injection. Journal of Cerebral Blood Flow and Metabolism 2011, 31:1403-1411.
67. Théberge J. Perfusion magnetic resonance imaging in psychiatry. Topics in Magnetic Resonance Imaging 2008, 19:111-130.
68. Tregellas J.R. Neuroimaging biomarkers for early drug development in schizophrenia. Biological Psychiatry 2014, 76:111-119.
69. van Osch M.J., van der Grond J., Bakker C.J. Partial volume effects on arterial input functions: shape and amplitude distortions and their correction. Journal of Magnetic Resonance Imaging 2005, 22:704-709.
70. Vita A., Bressi S., Perani D., Invernizzi G., Giobbio G.M., Dieci M., Garbarini M., Del Sole A., Fazio F. High-resolution SPECT study of regional cerebral blood flow in drug-free and drug-naive schizophrenic patients. The American Journal of Psychiatry 1995, 152:876-882.
71. Walther S., Federspiel A., Horn H., Razavi N., Wiest R., Dierks T., Strik W., Muller T.J. Resting state cerebral blood flow and objective motor activity reveal basal ganglia dysfunction in schizophrenia. Psychiatry Research: Neuroimaging 2011, 192:117-124.
72. Wang D.J., Alger J.R., Qiao J.X., Gunther M., Pope W.B., Saver J.L., Salamon N., Liebeskind D.S. Multi-delay multi-parametric arterial spin-labeled perfusion MRI in acute ischemic stroke - comparison with dynamic susceptibility contrast enhanced perfusion imaging. NeuroImage: Clinical 2013, 3:1-7.
73. White C.M., Pope W.B., Zaw T., Qiao J., Naeini K.M., Lai A., Nghiemphu P.L., Wang J.J., Cloughesy T.F., Ellingson B.M. Regional and voxel-wise comparisons of blood flow measurements between dynamic susceptibility contrast magnetic resonance imaging (DSC-MRI) and arterial spin labeling (ASL) in brain tumors. Journal of Neuroimaging 2014, 24:23-30.
74. Wintermark M., Sesay M., Barbier E., Borbely K., Dillon W.P., Eastwood J.D., Glenn T.C., Grandin C.B., Pedraza S., Soustiel J.F., Nariai T., Zaharchuk G., Caille J.M., Dousset V., Yonas H. Comparative overview of brain perfusion imaging techniques. Stroke 2005, 36:e83-e99.
75. Wu B., Lou X., Wu X., Ma L. Intra- and interscanner reliability and reproducibility of 3D whole-brain pseudo-continuous arterial spin-labeling MR perfusion at 3T. Journal of Magnetic Resonance Imaging 2014, 39:402-409.
76. Xu G., Rowley H.A., Wu G., Alsop D.C., Shankaranarayanan A., Dowling M., Christian B.T., Oakes T.R., Johnson S.C. Reliability and precision of pseudo-continuous arterial spin labeling perfusion MRI on 3.0T and comparison with 15O-water PET in elderly subjects at risk for Alzheimer[U+05F3]s disease. NMR in Biomedicine 2010, 23:286-293.
77. Zaharchuk G., El Mogy I.S., Fischbein N.J., Albers G.W. Comparison of arterial spin labeling and bolus perfusion-weighted imaging for detecting mismatch in acute stroke. Stroke 2012, 43:1843-1848.
78. Zaro-Weber O., Moeller-Hartmann W., Heiss W.D., Sobesky J. Influence of the arterial input function on absolute and relative perfusion-weighted imaging penumbral flow detection: a validation with (1)(5)O-water positron emission tomography. Stroke 2012, 43:378-385.
79. Zhang Z.J., Reynolds G.P. A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophrenia Research 2002, 55:1-10.