Reduced binding potential of GABA-A/benzodiazepine receptors in individuals at ultra-high risk for psychosis: An [18F]-fluoroflumazenil positron emission tomography study

Schizophrenia Bulletin

Volumn 40, Issue 3, 2014, Pages 548-557

  Kang, Jee In ^a,b   Park, Hae Jeong ^a,b   Kim, Se Joo ^a,b   Kim, Kyung Ran ^a,b   Lee, Su Young ^b,c   Lee, Eun ^a,b   An, Suk Kyoon ^a,b,d   Kwon, Jun Soo ^e   Lee, Jong Doo ^a  

^a Yonsei University College of Medicine   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

^c Kwandong University College of Medicine   (South Korea)

^d Yonsei University   (South Korea)

^e Seoul National University College of Medicine   (South Korea)

Author keywords

caudate; fluoroflumazenil; GABA; PET; risk for psychosis; schizophrenia; ultra high

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ARIPIPRAZOLE; BENZODIAZEPINE RECEPTOR; FLUOROFLUMAZENIL F 18; QUETIAPINE; RADIOPHARMACEUTICAL AGENT; RISPERIDONE; UNCLASSIFIED DRUG; 2'-FLUOROFLUMAZENIL; 4 AMINOBUTYRIC ACID; FLUMAZENIL; PROTEIN BINDING;

ADOLESCENT; ADULT; ARTICLE; CALIFORNIA VERBAL LEARNING TEST; CAUDATE NUCLEUS; CLINICAL ARTICLE; COGNITION; COMPUTER PROGRAM; CONTINUOUS PERFORMANCE TEST; CONTROLLED ORAL WORD ASSOCIATION TEST; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FIGURE FLUENCY TEST; FUNCTIONAL NEUROIMAGING; GABAERGIC TRANSMISSION; HIGH RISK PATIENT; HIPPOCAMPUS; HUMAN; MALE; MONTGOMERY ASBERG DEPRESSION RATING SCALE; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; NUCLEUS ACCUMBENS; PARAHIPPOCAMPAL GYRUS; PET-CT SCANNER; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PRODROMAL SYMPTOM; PSYCHOSIS; PUTAMEN; RECALL; RECEPTOR BINDING; STROOP TEST; STRUCTURED INTERVIEW; STRUCTURED INTERVIEW FOR PRODROMAL SYNDROME; ULTRA HIGH RISK PATIENT; WISCONSIN CARD SORTING TEST; YOUNG ADULT; ANALOGS AND DERIVATIVES; BRAIN; CASE CONTROL STUDY; METABOLISM; RISK; SCHIZOPHRENIA; SCINTISCANNING;

ADOLESCENT; BRAIN; CASE-CONTROL STUDIES; CAUDATE NUCLEUS; FEMALE; FLUMAZENIL; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; HUMANS; MALE; NUCLEUS ACCUMBENS; PARAHIPPOCAMPAL GYRUS; POSITRON-EMISSION TOMOGRAPHY; PRODROMAL SYMPTOMS; PROTEIN BINDING; PUTAMEN; RECEPTORS, GABA-A; RISK; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84899025505     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbt052     Document Type: Article

References (57)

1. Howes OD, Kapur S. The dopamine hypothesis of schizophrenia: Version III-The final common pathway. Schizophr Bull. 2009;35:549-562.
2. Lyon GJ, Abi-Dargham A, Moore H, Lieberman JA, Javitch JA, Sulzer D. Presynaptic regulation of dopamine transmission in schizophrenia. Schizophr Bull. 2011;37:108-117.
3. Benes FM. Neural circuitry models of schizophrenia: Is it dopamine, GABA, glutamate, or something elsé Biol Psychiatry. 2009;65:1003-1005.
4. Rolls ET, Loh M, Deco G, Winterer G. Computational models of schizophrenia and dopamine modulation in the prefrontal cortex. Nat Rev Neurosci. 2008;9:696-709.
5. Moghaddam B, Javitt D. From revolution to evolution: The glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology. 2012;37:4-15.
6. Olney JW, Farber NB. Glutamate receptor dysfunction and schizophrenia. Arch Gen Psychiatry. 1995;52:998-1007.
7. Volk D, Austin M, Pierri J, Sampson A, Lewis D. GABA transporter-1 mRNA in the prefrontal cortex in schizophrenia: Decreased expression in a subset of neurons. Am J Psychiatry. 2001;158:256-265.
8. Wassef A, Baker J, Kochan LD. GABA and schizophrenia: A review of basic science and clinical studies. J Clin Psychopharmacol. 2003;23:601-640.
9. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 2005;6: 312-324.
10. Beasley CL, Zhang ZJ, Patten I, Reynolds GP. Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium-binding proteins. Biol Psychiatry. 2002;52:708-715.
11. Hanada S, Mita T, Nishino N, Tanaka C. [3H]muscimol binding sites increased in autopsied brains of chronic schizophrenics. Life Sci. 1987;40:259-266.
12. Simpson MD, Slater P, Royston MC, Deakin JF. Regionally selective deficits in uptake sites for glutamate and gamma-Aminobutyric acid in the basal ganglia in schizophrenia. Psychiatry Res. 1992;42:273-282.
13. Veldic M, Kadriu B, Maloku E, et al. Epigenetic mechanisms expressed in basal ganglia GABAergic neurons differentiate schizophrenia from bipolar disorder. Schizophr Res. 2007;91:51-61.
14. Goto N, Yoshimura R, Moriya J, et al. Reduction of brain gamma-Aminobutyric acid (GABA) concentrations in early-stage schizophrenia patients: 3T Proton MRS study. Schizophr Res. 2009;112:192-193.
15. Sesack SR, Grace AA. Cortico-Basal Ganglia reward network: Microcircuitry. Neuropsychopharmacology. 2010;35:27-47.
16. Kreitzer AC. Physiology and pharmacology of striatal neurons. Annu Rev Neurosci. 2009;32:127-147.
17. Busatto GF, Pilowsky LS, Costa DC, et al. Correlation between reduced in vivo benzodiazepine receptor binding and severity of psychotic symptoms in schizophrenia. Am J Psychiatry. 1997;154:56-63.
18. Asai Y, Takano A, Ito H, et al. GABAA/benzodiazepine receptor binding in patients with schizophrenia using [11C] Ro15-4513, a radioligand with relatively high affinity for alpha5 subunit. Schizophr Res. 2008;99:333-340.
19. Yung AR, Nelson B, Stanford C, et al. Validation of 'prodromal' criteria to detect individuals at ultra high risk of psychosis: 2 year follow-up. Schizophr Res. 2008;105:10-17.
20. Woods SW, Addington J, Cadenhead KS, et al. Validity of the prodromal risk syndrome for first psychosis: Findings from the North American Prodrome Longitudinal Study. Schizophr Bull. 2009;35:894-908.
21. Stone JM, Howes OD, Egerton A, et al. Altered relationship between hippocampal glutamate levels and striatal dopamine function in subjects at ultra high risk of psychosis. Biol Psychiatry. 2010;68:599-602.
22. Howes OD, Montgomery AJ, Asselin MC, et al. Elevated striatal dopamine function linked to prodromal signs of schizophrenia. Arch Gen Psychiatry. 2009;66:13-20.
23. de la Fuente-Sandoval C, Leon-Ortiz P, Favila R, Stephano S, Mamo D, Ramirez-Bermudez J, et al. Higher levels of glutamate in the associative-striatum of subjects with prodromal symptoms of schizophrenia and patients with first-episode psychosis. Neuropsychopharmacology. 2011;36:1781-1791.
24. Salmi E, Aalto S, Hirvonen J, et al. Measurement of GABA(A) receptor binding in vivo with [C-11]flumazenil: A test-retest study in healthy subjects. Neuroimage. 2008;41:260-269.
25. Mitterhauser M, Wadsak W, Wabnegger L, et al. Biological evaluation of 2′-[18F]fluoroflumazenil ([18F]FFMZ), a potential GABA receptor ligand for PET. Nucl Med Biol. 2004;31:291-295.
26. Yoon YH, Jeong JM, Kim HW, et al. Novel one-pot onestep synthesis of 2′-[(18)F]fluoroflumazenil (FFMZ) for benzodiazepine receptor imaging. Nucl Med Biol. 2003;30: 521-527.
27. Jung MH, Jang JH, Kang DH, et al. The reliability and validity of the korean version of the structured interview for prodromal syndrome. Psychiatry Investig. 2010;7:257-263.
28. First RLS, Gibbon M, Williams JBW. Structured Clinical Interview for DSM-IV Axis I Disorders: Clinical Version (SCID-CV). Washington, DC: American Psychiatric Press; 1997.
29. McGlashan T, Miller T, Woods S, Rosen J, Hoffman R, Davidson L, eds. Structured Interview for Prodromal Syndromes (SIPS). Version 4.0. New Heaven: Yale University; 2003.
30. Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134:382-389.
31. Delis DC, Kramer JH, Kaplan E, Ober BA. The California Verbal Learning Test. San Antonio, TX: Psychological Corporation; 1987.
32. Nuechterlein KH, Edell WS, Norris M, Dawson ME. Attentional vulnerability indicators, thought disorder, and negative symptoms. Schizophr Bull. 1986;12:408-426.
33. Golden CJ. Stroop Color and Word Test: Manual for Clinical and Experimental Uses. Chicago, IL: Stoelting; 1978.
34. Heaton RK, Chelune GJ, Talley JL, Kay GG, Curtiss G. Wisconsin Card Sorting Test Manual: Revised and Expanded. Odessa, FL: Psychological Assessment Resources Inc; 1993.
35. Spreen O, Benton AL. Neurosensory Center Comprehensive Examination for Aphasia. Victoria, BC: University of Victoria Neuropsychology Laboratory; 1977.
36. Ruff RM. The ruff figural fluency test: A normative study with adults. Dev Neuropsychol. 1987(3):37-52.
37. Hawkins KA, Addington J, Keefe RS, et al. Neuropsychological status of subjects at high risk for a first episode of psychosis. Schizophr Res. 2004;67:115-122.
38. Ball S, Busatto GF, David AS, et al. Cognitive functioning and GABAA/benzodiazepine receptor binding in schizophrenia: A 123I-iomazenil SPET study. Biol Psychiatry. 1998;43: 107-117.
39. Lee JD, Park HJ, Park ES, et al. Assessment of regional GABA(A) receptor binding using 18F-fluoroflumazenil positron emission tomography in spastic type cerebral palsy. Neuroimage. 2007;34:19-25.
40. Ichise M, Ballinger JR, Golan H, et al. Noninvasive quantification of dopamine D2 receptors with iodine-123-IBF SPECT. J Nucl Med. 1996;37:513-520.
41. Innis RB, Cunningham VJ, Delforge J, et al. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab. 2007;27:1533-1539.
42. Klumpers UM, Veltman DJ, Boellaard R, et al. Comparison of plasma input and reference tissue models for analysing [(11)C]flumazenil studies. J Cereb Blood Flow Metab. 2008;28:579-587.
43. Millet P, Graf C, Buck A, Walder B, Ibanez V. Evaluation of the reference tissue models for PET and SPECT benzodiazepine binding parameters. Neuroimage. 2002;17:928-942.
44. Ward D. 2000. Simultaneous Inference for FMRI Data. AFNI AlphaSim documentation. Biophysics Research Institute, Medical College of Wisconsin; 2000.
45. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15:273-289.
46. Squires RF, Lajtha A, Saederup E, Palkovits M. Reduced [3H]flunitrazepam binding in cingulate cortex and hippocampus of postmortem schizophrenic brains: Is selective loss of glutamatergic neurons associated with major psychoses? Neurochem Res. 1993;18:219-223.
47. van Kammen DP, Sternberg DE, Hare TA, Waters RN, Bunney Jr. W.E. CSF levels of gamma-Aminobutyric acid in schizophrenia. Low values in recently ill patients. Arch Gen Psychiatry. 1982;39:91-97.
48. Abi-Dargham A, Laruelle M, Krystal J, et al. No evidence of altered in vivo benzodiazepine receptor binding in schizophrenia. Neuropsychopharmacology. 1999;20:650-661.
49. Benes FM, Khan Y, Vincent SL, Wickramasinghe R. Differences in the subregional and cellular distribution of GABAA receptor binding in the hippocampal formation of schizophrenic brain. Synapse. 1996;22:338-349.
50. Corson PW, Nopoulos P, Andreasen NC, Heckel D, Arndt S. Caudate size in first-episode neuroleptic-naive schizophrenic patients measured using an artificial neural network. Biol Psychiatry. 1999;46:712-720.
51. Keshavan MS, Rosenberg D, Sweeney JA, Pettegrew JW. Decreased caudate volume in neuroleptic-naive psychotic patients. Am J Psychiatry. 1998;155:774-778.
52. Mechelli A, Riecher-Rossler A, Meisenzahl EM, et al. Neuroanatomical abnormalities that predate the onset of psychosis: A multicenter study. Arch Gen Psychiatry. 2011;68:489-495.
53. Lujan R, Shigemoto R, Lopez-Bendito G. Glutamate and GABA receptor signalling in the developing brain. Neuroscience. 2005;130:567-580.
54. Zai CC, Tiwari AK, King N, et al. Association study of the gamma-Aminobutyric acid type a receptor gamma2 subunit gene with schizophrenia. Schizophr Res. 2009;114: 33-38.
55. Yee BK, Keist R, von Boehmer L, et al. A schizophreniarelated sensorimotor deficit links alpha 3-containing GABAA receptors to a dopamine hyperfunction. Proc Natl Acad Sci USA. 2005;102:17154-17159.
56. Frankle WG, Cho RY, Narendran R, et al. Tiagabine increases [11C]flumazenil binding in cortical brain regions in healthy control subjects. Neuropsychopharmacology. 2009;34: 624-633.
57. Kapur S, Mizrahi R, Li M. From dopamine to salience to psychosis-linking biology, pharmacology and phenomenology of psychosis. Schizophr Res. 2005;79:59-68.