Hippocampal-parietal dysconnectivity and glutamate abnormalities in unmedicated patients with schizophrenia

Hippocampus

Volumn 24, Issue 12, 2014, Pages 1524-1532

  Kraguljac, Nina Vanessa ^a   White, David Matthew ^a   Hadley, Jennifer ^a,b   Reid, Meredith Amanda ^a,b   Lahti, Adrienne Carol ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b and Radiation Oncology   (United States)

Author keywords

Default mode network; Functional magnetic resonance imaging; Magnetic resonance spectroscopy; Memory; Precuneus; Resting state

Indexed keywords

CREATINE; GLUTAMIC ACID; NEUROLEPTIC AGENT;

ADULT; ANTERIOR CINGULATE; ARTICLE; BRAIN REGION; BRIEF PSYCHIATRIC RATING SCALE; CEREBELLUM; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; INSULA; MALE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARAHIPPOCAMPAL GYRUS; PRECUNEUS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; PUTAMEN; RESTING STATE NETWORK; SCHIZOPHRENIA; SIGNAL NOISE RATIO; SUPERIOR TEMPORAL GYRUS; BRAIN MAPPING; IMAGE PROCESSING; METABOLISM; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; PATHOPHYSIOLOGY; REST;

ADULT; BRAIN MAPPING; CREATINE; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PARIETAL LOBE; PROTON MAGNETIC RESONANCE SPECTROSCOPY; REST; SCHIZOPHRENIA;

EID: 84911007980     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22332     Document Type: Article

References (61)

1. Ashburner J. 2007. A fast diffeomorphic image registration algorithm. Neuroimage 38:95-113.
2. Behzadi Y, Restom K, Liau J, Liu TT. 2007. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37:90-101.
3. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. 1995. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541.
4. Buckner RL, Andrews-Hanna JR, Schacter DL. 2008. The brain's default network: Anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1-38.
5. Bullmore E, Vertes P. 2013. From lichtheim to rich club: Brain networks and psychiatry. JAMA Psychiatry 70:780-782.
6. Calhoun VD, Kiehl KA, Pearlson GD. 2008. Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Hum Brain Mapp 29:828-838.
7. Carp J. 2011. Optimizing the order of operations for movement scrubbing: Comment on Power et al. Neuroimage 76:436-438.
8. Carpenter WT Jr., Gold JM, Lahti AC, Queern CA, Conley RR, Bartko JJ, Kovnick J, Appelbaum PS. 2000. Decisional capacity for informed consent in schizophrenia research. Arch Gen Psychiatry 57:533-538.
9. Cavanna AE, Trimble MR. 2006. The precuneus: A review of its functional anatomy and behavioural correlates. Brain 129(Pt 3):564-583.
10. D'Argembeau A, Collette F, Van der Linden M, Laureys S, Del Fiore G, Degueldre C, Luxen A, Salmon E. 2005. Self-referential reflective activity and its relationship with rest: A PET study. Neuroimage 25:616-624.
11. Duncan NW, Enzi B, Wiebking C, Northoff G. 2011. Involvement of glutamate in rest-stimulus interaction between perigenual and supragenual anterior cingulate cortex: A combined fMRI-MRS study. Hum Brain Mapp 32:2172-2182.
12. Duncan NW, Wiebking C, Tiret B, Marjanska M, Hayes DJ, Lyttleton O, Doyon J, Northoff G. 2013. Glutamate concentration in the medial prefrontal cortex predicts resting-state cortical-subcortical functional connectivity in humans. PLoS One 8:e60312.
13. Enzi B, Duncan NW, Kaufmann J, Tempelmann C, Wiebking C, Northoff G. 2012. Glutamate modulates resting state activity in the perigenual anterior cingulate cortex - a combined fMRI-MRS study. Neuroscience 227:102-109.
14. Falkenberg LE, Westerhausen R, Specht K, Hugdahl K. 2012. Resting-state glutamate level in the anterior cingulate predicts blood-oxygen level-dependent response to cognitive control. Proc Natl Acad Sci USA 109:5069-5073.
15. Flemenbaum A, Zimmermann RL. 1973. Inter- and intra-rater reliability of the brief psychiatric rating scale. Psychol Rep 32:783-792.
16. Gilbert SJ, Spengler S, Simons JS, Steele JD, Lawrie SM, Frith CD, Burgess PW. 2006. Functional specialization within rostral prefrontal cortex (area 10): A meta-analysis. J Cogn Neurosci 18:932-948.
17. Goveas JS, Xie C, Ward BD, Wu Z, Li W, Franczak M, Jones JL, Antuono PG, Li SJ. 2011. Recovery of hippocampal network connectivity correlates with cognitive improvement in mild Alzheimer's disease patients treated with donepezil assessed by resting-state fMRI. J Magn Reson Imaging 34:764-773.
18. Greicius MD, Krasnow B, Reiss AL, Menon V. 2003. Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100:253-258.
19. Gusnard DA, Akbudak E, Shulman GL, Raichle ME. 2001. Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proc Natl Acad Sci USA 98:4259-4264.
20. Hampson M, Driesen NR, Skudlarski P, Gore JC, Constable RT. 2006. Brain connectivity related to working memory performance. J Neurosci 26:13338-13343.
21. Holmes M, Folley BS, Sonmezturk HH, Gore JC, Kang H, Abou-Khalil B, Morgan VL. 2014. Resting state functional connectivity of the hippocampus associated with neurocognitive function in left temporal lobe epilepsy. Hum Brain Mapp 35:735-744.
22. Hutcheson NL, Reid MA, White DM, Kraguljac NV, Avsar KB, Bolding MS, Knowlton RC, den Hollander JA, Lahti AC. 2012. Multimodal analysis of the hippocampus in schizophrenia using proton magnetic resonance spectroscopy and functional magnetic resonance imaging. Schizophr Res 140:136-142.
23. Hyder F, Rothman DL, Shulman RG. 2002. Total neuroenergetics support localized brain activity: Implications for the interpretation of fMRI. Proc Natl Acad Sci USA 99:10771-10776.
24. Kapogiannis D, Reiter DA, Willette AA, Mattson MP. 2012. Posteromedial cortex glutamate and GABA predict intrinsic functional connectivity of the default mode network. Neuroimage 64C:112-119.
25. Kraguljac NV, Reid M, White D, Jones R, den Hollander J, Lowman D, Lahti AC. 2012a. Neurometabolites in schizophrenia and bipolar disorder - a systematic review and meta-analysis. Psychiatry Res 203:111-125.
26. Kraguljac NV, Reid MA, White DM, den Hollander J, Lahti AC. 2012b. Regional Decoupling of N-acetyl-aspartate and Glutamate in Schizophrenia. Neuropsychopharmacology 37:2635-2642.
27. Kraguljac NV, White DM, Reid MA, Lahti AC. 2013. Increased hippocampal glutamate and volumetric deficits in unmedicated patients with schizophrenia. JAMA Psychiatry 70:1294-1302.
28. Krystal JH, D'Souza DC, Mathalon D, Perry E, Belger A, Hoffman R. 2003. NMDA receptor antagonist effects, cortical glutamatergic function, and schizophrenia: Toward a paradigm shift in medication development. Psychopharmacology (Berl) 169:215-233.
29. Kuhn S, Gallinat J. 2013. Resting-state brain activity in schizophrenia and major depression: A quantitative meta-analysis. Schizophr Bull 39:358-365.
30. Lahti AC, Koffel B, LaPorte D, Tamminga CA. 1995. Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 13:9-19.
31. Liao W, Zhang Z, Pan Z, Mantini D, Ding J, Duan X, Luo C, Wang Z, Tan Q, Lu G, et al. 2011. Default mode network abnormalities in mesial temporal lobe epilepsy: A study combining fMRI and DTI. Hum Brain Mapp 32:883-895.
32. Lou HC, Luber B, Crupain M, Keenan JP, Nowak M, Kjaer TW, Sackeim HA, Lisanby SH. 2004. Parietal cortex and representation of the mental Self. Proc Natl Acad Sci USA 101:6827-6832.
33. Lowe MJ, Mock BJ, Sorenson JA. 1998. Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7:119-132.
34. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. 2003. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233-1239.
35. Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, Biswal BB, Villringer A, Castellanos FX, Milham MP, Petrides M. 2009. Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106:20069-20074.
36. Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN. 2007. Wandering minds: The default network and stimulus-independent thought. Science 315:393-395.
37. Nurnberger JI Jr., Blehar MC, Kaufmann CA, York-Cooler C, Simpson SG, Harkavy-Friedman J, Severe JB, Malaspina D, Reich T. 1994. Diagnostic interview for genetic studies. Rationale, unique features, and training. NIMH Genetics Initiative. Arch Gen Psychiatry 51:849-859; discussion 863-864.
38. Ongur D, Prescot AP, Jensen JE, Cohen BM, Renshaw PF. 2009. Creatine abnormalities in schizophrenia and bipolar disorder. Psychiatry Res 172:44-48.
39. Piekema C, Kessels RP, Rijpkema M, Fernandez G. 2009. The hippocampus supports encoding of between-domain associations within working memory. Learn Mem 16:231-234.
40. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. 2012. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142-2154.
41. Ragland JD, Laird AR, Ranganath C, Blumenfeld RS, Gonzales SM, Glahn DC. 2009. Prefrontal activation deficits during episodic memory in schizophrenia. Am J Psychiatry 166:863-874.
42. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. 2001. A default mode of brain function. Proc Natl Acad Sci USA 98:676-682.
43. Raj D, Anderson AW, Gore JC. 2001. Respiratory effects in human functional magnetic resonance imaging due to bulk susceptibility changes. Phys Med Biol 46:3331-3340.
44. Randolph C, Tierney MC, Mohr E, Chase TN. 1998. The repeatable battery for the assessment of neuropsychological status (RBANS): Preliminary clinical validity. J Clin Exp Neuropsychol 20:310-319.
45. Ranganath C, Heller A, Cohen MX, Brozinsky CJ, Rissman J. 2005. Functional connectivity with the hippocampus during successful memory formation. Hippocampus 15:997-1005.
46. Scheidegger M, Walter M, Lehmann M, Metzger C, Grimm S, Boeker H, Boesiger P, Henning A, Seifritz E. 2012. Ketamine decreases resting state functional network connectivity in healthy subjects: Implications for antidepressant drug action. PLoS One 7:e44799.
47. Schubert F, Gallinat J, Seifert F, Rinneberg H. 2004. Glutamate concentrations in human brain using single voxel proton magnetic resonance spectroscopy at 3 Tesla. Neuroimage 21:1762-1771.
48. Skudlarski P, Jagannathan K, Anderson K, Stevens MC, Calhoun VD, Skudlarska BA, Pearlson G. 2010. Brain connectivity is not only lower but different in schizophrenia: A combined anatomical and functional approach. Biol Psychiatry 68:61-69.
49. Smith AJ, Blumenfeld H, Behar KL, Rothman DL, Shulman RG, Hyder F. 2002. Cerebral energetics and spiking frequency: The neurophysiological basis of fMRI. Proc Natl Acad Sci USA 99:10765-10770.
50. Tamminga CA, Southcott S, Sacco C, Wagner AD, Ghose S. 2012. Glutamate dysfunction in hippocampus: Relevance of dentate gyrus and CA3 signaling. Schizophr Bull 38:927-935.
51. Tregellas JR, Smucny J, Harris JG, Olincy A, Maharajh K, Kronberg E, Eichman LC, Lyons E, Freedman R. 2014. Intrinsic hippocampal activity as a biomarker for cognition and symptoms in schizophrenia. Am J Psychiatry 171:549-556.
52. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M. 2002. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273-289.
53. Uddin LQ, Kelly AM, Biswal BB, Castellanos FX, Milham MP. 2009. Functional connectivity of default mode network components: Correlation, anticorrelation, and causality. Hum Brain Mapp 30:625-637.
54. van den Heuvel MP, Kahn RS, Goni J, Sporns O. 2012. High-cost, high-capacity backbone for global brain communication. Proc Natl Acad Sci USA 109:11372-11377.
55. van den Heuvel MP, Sporns O, Collin G, Scheewe T, Mandl RC, Cahn W, Goni J, Hulshoff Pol HE, Kahn RS. 2013. Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70:783-792.
56. Vanhamme L, van den Boogaart A, Van Huffel S. 1997. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129:35-43.
57. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. 2004. Fiber tract-based atlas of human white matter anatomy. Radiology 230:77-87.
58. Whitfield-Gabrieli S, Ford JM. 2012. Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol 8:49-76.
59. Whitfield-Gabrieli S, Thermenos HW, Milanovic S, Tsuang MT, Faraone SV, McCarley RW, Shenton ME, Green AI, Nieto-Castanon A, LaViolette P and others. 2009. Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc Natl Acad Sci USA 106:1279-1284.
60. Zarei M, Beckmann CF, Binnewijzend MA, Schoonheim MM, Oghabian MA, Sanz-Arigita EJ, Scheltens P, Matthews PM, Barkhof F. 2012. Functional segmentation of the hippocampus in the healthy human brain and in Alzheimer's disease. Neuroimage 66C:28-35.
61. Zhou Y, Shu N, Liu Y, Song M, Hao Y, Liu H, Yu C, Liu Z, Jiang T. 2008. Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr Res 100:120-132.