Imaging Patients with Psychosis and a Mouse Model Establishes a Spreading Pattern of Hippocampal Dysfunction and Implicates Glutamate as a Driver

Neuron

Volumn 78, Issue 1, 2013, Pages 81-93

  Schobel, Scott A ^a,b,f   Chaudhury, Nashid H ^b,g   Khan, Usman A ^a,c   Paniagua, Beatriz ^d   Styner, Martin A ^d,e   Asllani, Iris ^a   Inbar, Benjamin P ^b   Corcoran, Cheryl M ^a,b   Lieberman, Jeffrey A ^a,b   Moore, Holly ^a   Small, Scott A ^a  

^a NewYork Presbyterian Hospital   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c SUNY DOWNSTATE MEDICAL CENTER   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e Brooks Computer Science Building   (United States)

^f F HOFFMANN LA ROCHE LTD   (Switzerland)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; GLUTAMIC ACID; KETAMINE; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN BLOOD FLOW; BRAIN MAPPING; BRAIN METABOLISM; BRAIN SIZE; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ASSOCIATION; ENTORHINAL CORTEX; FOLLOW UP; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GABAERGIC TRANSMISSION; HIGH RISK PATIENT; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HISTOPATHOLOGY; HUMAN; HYPERMETABOLISM; IN VIVO STUDY; INTERNEURON; LONGITUDINAL STUDY; MALE; MOLECULAR PATHOLOGY; MORPHOMETRICS; MOUSE; NEUROIMAGING; NEUROPATHOLOGY; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; PSYCHOSIS; STRUCTURE ANALYSIS; SUBICULUM;

AMINO ACIDS; ANIMALS; ATROPHY; BICYCLO COMPOUNDS, HETEROCYCLIC; BRAIN MAPPING; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; FOLLOW-UP STUDIES; FUNCTIONAL LATERALITY; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; IMAGING, THREE-DIMENSIONAL; KETAMINE; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; PSYCHOTIC DISORDERS; TIME FACTORS;

EID: 84876084495     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.02.011     Document Type: Article

References (63)

1. Andreasen N.C., Nopoulos P., Magnotta V., Pierson R., Ziebell S., Ho B.C. Progressive brain change in schizophrenia: a prospective longitudinal study of first-episode schizophrenia. Biol. Psychiatry 2011, 70:672-679.
2. Behrens M.M., Ali S.S., Dao D.N., Lucero J., Shekhtman G., Quick K.L., Dugan L.L. Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 2007, 318:1645-1647.
3. Benes F.M. Evidence for altered trisynaptic circuitry in schizophrenic hippocampus. Biol. Psychiatry 1999, 46:589-599.
4. Benneyworth M.A., Roseman A.S., Basu A.C., Coyle J.T. Failure of NMDA receptor hypofunction to induce a pathological reduction in PV-positive GABAergic cell markers. Neurosci. Lett. 2011, 488:267-271.
5. Bickel S., Javitt D.C. Neurophysiological and neurochemical animal models of schizophrenia: focus on glutamate. Behav. Brain Res. 2009, 204:352-362.
6. Cannon T.D., Cadenhead K., Cornblatt B., Woods S.W., Addington J., Walker E., Seidman L.J., Perkins D., Tsuang M., McGlashan T., Heinssen R. Prediction of psychosis in youth at high clinical risk: a multisite longitudinal study in North America. Arch. Gen. Psychiatry 2008, 65:28-37.
7. Cartmell J., Monn J.A., Schoepp D.D. The metabotropic glutamate 2/3 receptor agonists LY354740 and LY379268 selectively attenuate phencyclidine versus d-amphetamine motor behaviors in rats. J. Pharmacol. Exp. Ther. 1999, 291:161-170.
8. Coultrap S.J., Nixon K.M., Alvestad R.M., Valenzuela C.F., Browning M.D. Differential expression of NMDA receptor subunits and splice variants among the CA1, CA3 and dentate gyrus of the adult rat. Brain Res. Mol. Brain Res. 2005, 135:104-111.
9. Csernansky J.G., Joshi S., Wang L., Haller J.W., Gado M., Miller J.P., Grenander U., Miller M.I. Hippocampal morphometry in schizophrenia by high dimensional brain mapping. Proc. Natl. Acad. Sci. USA 1998, 95:11406-11411.
10. de la Fuente-Sandoval C., León-Ortiz P., Favila R., Stephano S., Mamo D., Ramírez-Bermúdez J., Graff-Guerrero A. 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.
11. Rothman D.L., Hyder F., Sibson N., Behar K.L., Mason G.F., Shen J., Petroff O.A.C., Shulman R.G. In vivo magnetic resonance spectroscopy studies of the glutamate and GABA neurotransmitter cycles and functional neuroenergetics. Neuropsychopharmacology: The Fifth Generation of Progress 2002, Lippencott Williams & Wilkins, Philadelphia, PA. K.L. Davis (Ed.).
12. Fusar-Poli P., Bonoldi I., Yung A.R., Borgwardt S., Kempton M.J., Valmaggia L., Barale F., Caverzasi E., McGuire P. Predicting psychosis: meta-analysis of transition outcomes in individuals at high clinical risk. Arch. Gen. Psychiatry 2012, 69:220-229.
13. Gaisler-Salomon I., Miller G.M., Chuhma N., Lee S., Zhang H., Ghoddoussi F., Lewandowski N., Fairhurst S., Wang Y., Conjard-Duplany A., et al. Glutaminase-deficient mice display hippocampal hypoactivity, insensitivity to pro-psychotic drugs and potentiated latent inhibition: relevance to schizophrenia. Neuropsychopharmacology 2009, 34:2305-2322.
14. Gao X.M., Sakai K., Roberts R.C., Conley R.R., Dean B., Tamminga C.A. Ionotropic glutamate receptors and expression of N-methyl-D-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia. Am. J. Psychiatry 2000, 157:1141-1149.
15. González R.G., Fischman A.J., Guimaraes A.R., Carr C.A., Stern C.E., Halpern E.F., Growdon J.H., Rosen B.R. Functional MR in the evaluation of dementia: correlation of abnormal dynamic cerebral blood volume measurements with changes in cerebral metabolism on positron emission tomography with fludeoxyglucose F 18. AJNR Am. J. Neuroradiol. 1995, 16:1763-1770.
16. Gozzi A., Large C.H., Schwarz A., Bertani S., Crestan V., Bifone A. Differential effects of antipsychotic and glutamatergic agents on the phMRI response to phencyclidine. Neuropsychopharmacology 2008, 33:1690-1703.
17. Greene R. Circuit analysis of NMDAR hypofunction in the hippocampus, in vitro, and psychosis of schizophrenia. Hippocampus 2001, 11:569-577.
18. Harrison P.J. The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology (Berl.) 2004, 174:151-162.
19. Heckers S., Konradi C. Hippocampal pathology in schizophrenia. Curr. Top Behav. Neurosci. 2010, 4:529-553.
20. 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. Nat. Neurosci. 1998, 1:318-323.
21. Hu Y., Mitchell K.M., Albahadily F.N., Michaelis E.K., Wilson G.S. Direct measurement of glutamate release in the brain using a dual enzyme-based electrochemical sensor. Brain Res. 1994, 659:117-125.
22. Imre G., Salomons A., Jongsma M., Fokkema D.S., Den Boer J.A., Ter Horst G.J. Effects of the mGluR2/3 agonist LY379268 on ketamine-evoked behaviours and neurochemical changes in the dentate gyrus of the rat. Pharmacol. Biochem. Behav. 2006, 84:392-399.
23. Jentsch J.D., Roth R.H. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999, 20:201-225.
24. Kawasaki Y., Suzuki M., Maeda Y., Urata K., Yamaguchi N., Matsuda H., Hisada K., Suzuki M., Takashima T. Regional cerebral blood flow in patients with schizophrenia. A preliminary report. Eur. Arch. Psychiatry Clin. Neurosci. 1992, 241:195-200.
25. Keilhoff G., Becker A., Grecksch G., Wolf G., Bernstein H.G. Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those found in human schizophrenia. Neuroscience 2004, 126:591-598.
26. Krystal J.H., Karper L.P., Seibyl J.P., Freeman G.K., Delaney R., Bremner J.D., Heninger G.R., Bowers M.B., Charney D.S. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch. Gen. Psychiatry 1994, 51:199-214.
27. Krystal J.H., Abi-Saab W., Perry E., D'Souza D.C., Liu N., Gueorguieva R., McDougall L., Hunsberger T., Belger A., Levine L., Breier A. Preliminary evidence of attenuation of the disruptive effects of the NMDA glutamate receptor antagonist, ketamine, on working memory by pretreatment with the group II metabotropic glutamate receptor agonist, LY354740, in healthy human subjects. Psychopharmacology (Berl.) 2005, 179:303-309.
28. Kühn S., Musso F., Mobascher A., Warbrick T., Winterer G., Gallinat J. Hippocampal subfields predict positive symptoms in schizophrenia: first evidence from brain morphometry. Transcult. Psychiatry 2012, 2:e127.
29. Laviola G., Macrì S., Morley-Fletcher S., Adriani W. Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci. Biobehav. Rev. 2003, 27:19-31.
30. Law A.J., Deakin J.F. Asymmetrical reductions of hippocampal NMDAR1 glutamate receptor mRNA in the psychoses. Neuroreport 2001, 12:2971-2974.
31. Liao Y., Tang J., Corlett P.R., Wang X., Yang M., Chen H., Liu T., Chen X., Hao W., Fletcher P.C. Reduced dorsal prefrontal gray matter after chronic ketamine use. Biol. Psychiatry 2011, 69:42-48.
32. Lin W., Celik A., Paczynski R.P. Regional cerebral blood volume: a comparison of the dynamic imaging and the steady state methods. J. Magn. Reson. Imaging 1999, 9:44-52.
33. 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 Neurosci. 2008, 31:234-242.
34. Lorrain D.S., Baccei C.S., Bristow L.J., Anderson J.J., Varney M.A. Effects of ketamine and N-methyl-D-aspartate on glutamate and dopamine release in the rat prefrontal cortex: modulation by a group II selective metabotropic glutamate receptor agonist LY379268. Neuroscience 2003, 117:697-706.
35. 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. Biol. Psychiatry 2004, 56:931-937.
36. Malhotra A.K., Pinals D.A., Adler C.M., Elman I., Clifton A., Pickar D., Breier A. Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology 1997, 17:141-150.
37. 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.
38. Miller T.J., McGlashan T.H., Rosen J.L., Cadenhead K., Cannon T., Ventura J., McFarlane W., Perkins D.O., Pearlson G.D., Woods S.W. Prodromal assessment with the structured interview for prodromal syndromes and the scale of prodromal symptoms: predictive validity, interrater reliability, and training to reliability. Schizophr. Bull. 2003, 29:703-715.
39. Moghaddam B., Adams B.W. Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 1998, 281:1349-1352.
40. Moghaddam B., Javitt D. From revolution to evolution: the glutamate hypothesis of schizophrenia and its implication for treatment. Neuropsychopharmacology 2012, 37:4-15.
41. Moghaddam B., Adams B., Verma A., Daly D. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J. Neurosci. 1997, 17:2921-2927.
42. Molina V., Reig S., Pascau J., Sanz J., Sarramea F., Gispert J.D., Luque R., Benito C., Palomo T., Desco M. Anatomical and functional cerebral variables associated with basal symptoms but not risperidone response in minimally treated schizophrenia. Psychiatry Res. 2003, 124:163-175.
43. Monn J.A., Valli M.J., Massey S.M., Hansen M.M., Kress T.J., Wepsiec J.P., Harkness A.R., Grutsch J.L., Wright R.A., Johnson B.G., et al. Synthesis, pharmacological characterization, and molecular modeling of heterobicyclic amino acids related to (+)-2-aminobicyclo[3.1.0] hexane-2,6-dicarboxylic acid (LY354740): identification of two new potent, selective, and systemically active agonists for group II metabotropic glutamate receptors. J. Med. Chem. 1999, 42:1027-1040.
44. Moreno H., Hua F., Brown T., Small S. Longitudinal mapping of mouse cerebral blood volume with MRI. NMR Biomed. 2006, 19:535-543.
45. 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. Arch. Neurol. 2007, 64:1467-1477.
46. Morey R.A., Petty C.M., Xu Y., Hayes J.P., Wagner H.R., Lewis D.V., LaBar K.S., Styner M., McCarthy G. A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes. Neuroimage 2009, 45:855-866.
47. Mouri A., Noda Y., Enomoto T., Nabeshima T. Phencyclidine animal models of schizophrenia: approaches from abnormality of glutamatergic neurotransmission and neurodevelopment. Neurochem. Int. 2007, 51:173-184.
48. Narr K.L., Thompson P.M., Szeszko P., Robinson D., Jang S., Woods R.P., Kim S., Hayashi K.M., Asunction D., Toga A.W., Bilder R.M. Regional specificity of hippocampal volume reductions in first-episode schizophrenia. Neuroimage 2004, 21:1563-1575.
49. Paus T., Keshavan M., Giedd J.N. Why do many psychiatric disorders emerge during adolescence?. Nat. Rev. Neurosci. 2008, 9:947-957.
50. Paxinos G., Franklin K. The Mouse Brain in Stereotaxic Coordinates 2001, Elsevier Academic Press, Amsterdam. Third Edition.
51. Pellerin L., Magistretti P.J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. USA 1994, 91:10625-10629.
52. Pinault D. N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex. Biol. Psychiatry 2008, 63:730-735.
53. Raichle M.E. Positron emission tomography. Annu. Rev. Neurosci. 1983, 6:249-267.
54. Sawiak S.J., Wood N.I., Williams G.B., Morton A.J., Carpenter T.A. Voxel-based morphometry in the R6/2 transgenic mouse reveals differences between genotypes not seen with manual 2D morphometry. Neurobiol. Dis. 2009, 33:20-27.
55. Schobel S.A., Kelly M.A., Corcoran C.M., Van Heertum K., Seckinger R., Goetz R., Harkavy-Friedman J., Malaspina D. Anterior hippocampal and orbitofrontal cortical structural brain abnormalities in association with cognitive deficits in schizophrenia. Schizophr. Res. 2009, 114:110-118.
56. 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. Arch. Gen. Psychiatry 2009, 66:938-946.
57. 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. Nat. Rev. Neurosci. 2011, 12:585-601.
58. Steen R.G., Mull C., McClure R., Hamer R.M., Lieberman J.A. Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br. J. Psychiatry 2006, 188:510-518.
59. Stone J.M., Dietrich C., Edden R., Mehta M.A., De Simoni S., Reed L.J., Krystal J.H., Nutt D., Barker G.J. Ketamine effects on brain GABA and glutamate levels with 1H-MRS: relationship to ketamine-induced psychopathology. Mol. Psychiatry 2012, 17:664-665.
60. Styner M., Lieberman J.A., Pantazis D., Gerig G. Boundary and medial shape analysis of the hippocampus in schizophrenia. Med. Image Anal. 2003, 8:197-203.
61. Styner M., Oguz I., Xu S., Pantazis D., Gerig G. Statistical group differences in anatomical shape analysis using Hotelling T2 metric. Proc. SPIE Medical Imaging 2007: Image Processing 2007, 6512:1-11.
62. Vutskits L., Gascon E., Potter G., Tassonyi E., Kiss J.Z. Low concentrations of ketamine initiate dendritic atrophy of differentiated GABAergic neurons in culture. Toxicology 2007, 234:216-226.
63. Yushkevich P.A., Piven J., Hazlett H.C., Smith R.G., Ho S., Gee J.C., Gerig G. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 2006, 31:1116-1128.