Relationship among glutamine, γ-aminobutyric acid, and social cognition in autism spectrum disorders

Journal of Child and Adolescent Psychopharmacology

Volumn 25, Issue 4, 2015, Pages 314-322

  Cochran, David M ^a   Sikoglu, Elif M ^a   Hodge, Steven M ^a   Edden, Richard A E ^b,c   Foley, Ann ^a   Kennedy, David N ^a   Moore, Constance M ^a   Frazier, Jean A ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CHOLINE; CREATINE; GLUTAMIC ACID; GLUTAMINE; INOSITOL; LISDEXAMFETAMINE; METHYLPHENIDATE; CREATININE;

ADOLESCENT; ANTERIOR CINGULATE; ANXIETY; ARTICLE; ASSESSMENT OF HUMANS; ATTENTION DISTURBANCE; AUTISM; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; DEPRESSION; HUMAN; INTELLIGENCE QUOTIENT; MALE; NEUROIMAGING; NEUROTRANSMISSION; POINT RESOLVED SPECTROSCOPY SEQUENCE; PROTON NUCLEAR MAGNETIC RESONANCE; PSYCHOSOCIAL WITHDRAWAL; READING THE MIND IN THE EYES TEST; SOCIAL COGNITION; SOCIAL PROBLEM; SOCIAL RESPONSIVENESS SCALE; THOUGHT DISORDER; CHEMISTRY; CINGULATE GYRUS; COGNITION; INTELLIGENCE; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PSYCHOLOGY;

ADOLESCENT; AUTISM SPECTRUM DISORDER; COGNITION; CREATININE; GAMMA-AMINOBUTYRIC ACID; GLUTAMINE; GYRUS CINGULI; HUMANS; INTELLIGENCE; MAGNETIC RESONANCE SPECTROSCOPY; MALE;

EID: 84929584646     PISSN: 10445463     EISSN: 15578992     Source Type: Journal    
DOI: 10.1089/cap.2014.0112     Document Type: Article

References (68)

1. Achenbach TM, Rescorla L: The Manual for the ASEBA School-Age Forms and Profiles. Burlington (VT), University of Vermont, Research Center for Children, Youth & Families, 2001.
2. Agam Y, Joseph RM, Barton JJ, Manoach DS: Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders. Neuroimage 52:336-347, 2010.
3. American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders, 4th ed. Washington, DC: American Psychiatric Association; 1994.
4. American Psychiatric Association: Statistical Manual of Mental Disorders, 5th ed. Washington, DC: American Psychiatric Association; 2013.
5. Autism and Developmental Disabilities Monitoring Network Surveillance Year 2008 Principal Investigators and Centers for Disease Control and Prevention: Prevalence of autism spectrum disorders-autism and developmental disabilities monitoring network, 14 sites, United States, 2008. MMWR Surveill Summ 61:1-19, 2012.
6. Bak LK, Schousboe A, Waagepetersen HS: The glutamate/GABA-glutamine cycle: Aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98:641-653, 2006.
7. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I: The "reading the mind in the eyes" test revised version: A study with normal adults, and adults with asperger syndrome or highfunctioning autism. J Child Psychol Psychiatry 42:241-251, 2001.
8. Bejjani A, O'Neill J, Kim JA, Frew AJ, Yee VW, Ly R, Kitchen C, Salamon N, McCracken JT, Toga AW, Alger JR, Levitt JG: Elevated glutamatergic compounds in pregenual anterior cingulate in pediatric autism spectrum disorder demonstrated by 1H MRS and 1H MRSI. PLoS One 7:e38786, 2012.
9. Bernardi S, Anagnostou E, Shen J, Kolevzon A, Buxbaum JD, Hollander E, Hof PR, Fan J: In vivo 1H-magnetic resonance spectroscopy study of the attentional networks in autism. Brain Res 1380:198-205, 2011.
10. Berry-Kravis EM, Hessl D, Rathmell B, Zarevics P, Cherubini M, Walton-Bowen K, Mu Y, Nguyen DV, Gonzalez-Heydrich J, Wang PP, Carpenter RL, Bear MF, Hagerman RJ: Effects of STX209 (arbaclofen) on neurobehavioral function in children and adults with fragile X syndrome: A randomized, controlled, phase 2 trial. Sci Transl Med 4:152ra127, 2012.
11. Blumberg SJ, Bramlett MD, Kogan MD, Schieve LA, Jones JR, Lu MC: Changes in prevalence of parent-reported autism spectrum disorders in school-aged U. S. children: 2007 to 2011-2012. National Health Statistics Reports No. 65; Hyattsville (MD), National Center for Health Statistics, 2013.
12. Brown MS, Singel D, Hepburn S, Rojas DC: Increased glutamate concentration in the auditory cortex of persons with autism and first-degree relatives: A (1) H-MRS study. Autism Res 6:1-10, 2013.
13. Constantino J, Gruber C: Social responsiveness scale (SRS). Los Angeles, Western Psychological Services, 2005.
14. DeVito TJ, Drost DJ, Neufeld RW, Rajakumar N, Pavlosky W, Williamson P, Nicolson R: Evidence for cortical dysfunction in autism: A proton magnetic resonance spectroscopic imaging study. Biol Psychiatry 61:465-473, 2007.
15. Dydak U, Jiang YM, Long LL, Zhu H, Chen J, Li WM, Edden RA, Hu S, Fu X, Long Z, Mo XA, Meier D, Harezlak J, Aschner M, Murdoch JB, Zheng W: In vivo measurement of brain GABA concentrations by magnetic resonance spectroscopy in smelters occupationally exposed to manganese. Environ Health Perspect 119:219-224, 2011.
16. Edden RA, Barker PB: Spatial effects in the detection of gammaaminobutyric acid: Improved sensitivity at high fields using inner volume saturation. Magn Reson Med 58:1276-1282, 2007.
17. Edden RA, Crocetti D, Zhu H, Gilbert DL, Mostofsky SH: Reduced GABA concentration in attention-deficit/hyperactivity disorder. Arch Gen Psychiatry 69:750-753, 2012.
18. Edden R A E, Puts N A J, Harris AD, Barker PB, Evans CJ: Gannet: A batch-processing tool for the quantitative analysis of gammaaminobutyric acid? edited MR spectroscopy spectra. J Magn Reson Imaging 40:1445-1452, 2014.
19. Edmonson C, Ziats MN, Rennert OM: Altered glial marker expression in autistic post-mortem prefrontal cortex and cerebellum. Mol Autism 5:3, 2014.
20. Enticott PG, Fitzgibbon BM, Kennedy HA, Arnold SL, Elliot D, Peachey A, Zangen A, Fitzgerald PB: A double-blind, randomized trial of deep repetitive transcranial magnetic stimulation (rTMS) for autism spectrum disorder. Brain Stimul 7:206-211, 2014.
21. Fatemi SH: The hyperglutamatergic hypothesis of autism. Prog Neuropsychopharmacol Biol Psychiatry 32:911-912, 2008.
22. Fatemi SH, Folsom TD: Dysregulation of fragile x mental retardation protein and metabotropic glutamate receptor 5 in superior frontal cortex of individuals with autism: A postmortem brain study. Mol Autism 2:6, 2011.
23. Fatemi SH, Folsom TD, Reutiman TJ, Thuras PD: Expression of GABA (B) receptors is altered in brains of subjects with autism. Cerebellum 8:64-69, 2009a.
24. Fatemi SH, Reutiman TJ, Folsom TD, Thuras PD: GABA (A) receptor downregulation in brains of subjects with autism. J Autism Dev Disord 39:223-230, 2009b.
25. Gaetz W, Bloy L, Wang DJ, Port RG, Blaskey L, Levy SE, Roberts TP: GABA estimation in the brains of children on the autism spectrum: Measurement precision and regional cortical variation. Neuroimage 86:1-9, 2014.
26. Gasparovic C, Song T, Devier D, Bockholt HJ, Caprihan A, Mullins PG, Posse S, Jung RE, Morrison LA: Use of tissue water as a concentration reference for proton spectroscopic imaging. Magn Reson Med 55:1219-1226, 2006.
27. Golembiowska K, Dziubina A: Effect of acute and chronic administration of citalopram on glutamate and aspartate release in the rat prefrontal cortex. Pol J Pharmacol 52:441-448, 2000.
28. Goto N, Yoshimura R, Kakeda S, Nishimura J, Moriya J, Hayashi K, Katsuki A, Hori H, Umene-Nakano W, Ikenouchi-Sugita A, Korogi Y, Nakamura J: Six-month treatment with atypical antipsychotic drugs decreased frontal-lobe levels of glutamate plus glutamine in early-stage first-episode schizophrenia. Neuropsychiatr Dis Treat 8:119-122, 2012.
29. Guastella AJ, Einfeld SL, Gray KM, Rinehart NJ, Tonge BJ, Lambert TJ, Hickie IB: Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol Psychiatry 67:692-694, 2010.
30. Hammerness P, Biederman J, Petty C, Henin A, Moore CM: Brain biochemical effects of methylphenidate treatment using proton magnetic spectroscopy in youth with attention-deficit hyperactivity disorder: A controlled pilot study. CNS Neurosci Ther 18:34-40, 2012.
31. Harada M, Taki MM, Nose A, Kubo H, Mori K, Nishitani H, Matsuda T: Non-invasive evaluation of the GABAergic/glutamatergic system in autistic patients observed by MEGA-editing proton MR spectroscopy using a clinical 3 tesla instrument. J Autism Dev Disord 41:447-454, 2011.
32. Haznedar MM, Buchsbaum MS, Wei TC, Hof PR, Cartwright C, Bienstock CA, Hollander E: Limbic circuitry in patients with autism spectrum disorders studied with positron emission tomography and magnetic resonance imaging. Am J Psychiatry 157:1994-2001, 2000.
33. Horder J, Lavender T, Mendez MA, O'Gorman R, Daly E, Craig MC, Lythgoe DJ, Barker GJ, Murphy DG: Reduced subcortical glutamate/glutamine in adults with autism spectrum disorders: A [(1) H]MRS study. Transl Psychiatry 3:e279, 2013.
34. Hothorn K, Hornik K, van de Wiel MA, Zeileis A: Implementing a class of permutation tests: The coin package. J Stat Softw 28:1-23, 2008.
35. Hothorn T, Hornik K, van de Wiel MA, Zeileis A: A lego system for conditional inference. Am Stat 60:257-263, 2006.
36. Howlin P, Moss P, Savage S, Rutter M: Social outcomes in mid- to later adulthood among individuals diagnosed with autism and average nonverbal IQ as children. J Am Acad Child Adolesc Psychiatry 52:572-81.e1, 2013.
37. Hyde KL, Samson F, Evans AC, Mottron L: Neuroanatomical differences in brain areas implicated in perceptual and other core features of autism revealed by cortical thickness analysis and voxelbased morphometry. Hum Brain Mapp 31:556-566, 2010.
38. Iltis I, Koski DM, Eberly LE, Nelson CD, Deelchand DK, Valette J, Ugurbil K, Lim KO, Henry PG: Neurochemical changes in the rat prefrontal cortex following acute phencyclidine treatment: An in vivo localized (1) H MRS study. NMR Biomed 22:737-744, 2009.
39. Jacquemont S, Curie A, des Portes V, Torrioli MG, Berry-Kravis E, Hagerman RJ, Ramos FJ, Cornish K, He Y, Paulding C, Neri G, Chen F, Hadjikhani N, Martinet D, Meyer J, Beckmann JS, Delange K, Brun A, Bussy G, Gasparini F, Hilse T, Floesser A, Branson J, Bilbe G, Johns D, Gomez-Mancilla B: Epigenetic modification of the FMR1 gene in fragile X syndrome is associated with differential response to the mGluR5 antagonist AFQ056. Sci Transl Med 3:64ra1, 2011.
40. Joshi G, Biederman J, Wozniak J, Goldin RL, Crowley D, Furtak S, Lukas SE, Gonenc A: Magnetic resonance spectroscopy study of the glutamatergic system in adolescent males with high-functioning autistic disorder: A pilot study at 4T. Eur Arch Psychiatry Clin Neurosci 263:379-384, 2013.
41. Magistretti PJ, Pellerin L: Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc Lond B Biol Sci 354:1155-1163, 1999.
42. Mescher M, Merkle H, Kirsch J, Garwood M, Gruetter R: Simultaneous in vivo spectral editing and water suppression. NMR Biomed 11:266-272, 1998.
43. Miller GA, Chapman JP: Misunderstanding analysis of covariance. J Abnorm Psychol 110:40-48, 2001.
44. Mlynarik V, Kohler I, Gambarota G, Vaslin A, Clarke PG, Gruetter R: Quantitative proton spectroscopic imaging of the neurochemical profile in rat brain with microliter resolution at ultra-short echo times. Magn Reson Med 59:52-58, 2008.
45. Mundy P: Annotation: The neural basis of social impairments in autism: The role of the dorsal medial-frontal cortex and anterior cingulate system. J Child Psychol Psychiatry 44:793-809, 2003.
46. Musazzi L, Milanese M, Farisello P, Zappettini S, Tardito D, Barbiero VS, Bonifacino T, Mallei A, Baldelli P, Racagni G, Raiteri M, Benfenati F, Bonanno G, Popoli M: Acute stress increases depolarizationevoked glutamate release in the rat prefrontal/frontal cortex: The dampening action of antidepressants. PLoS One 5:e8566, 2010.
47. Oblak A, Gibbs TT, Blatt GJ: Decreased GABAA receptors and benzodiazepine binding sites in the anterior cingulate cortex in autism. Autism Res 2:205-219, 2009.
48. Oblak AL, Gibbs TT, Blatt GJ: Decreased GABA (B) receptors in the cingulate cortex and fusiform gyrus in autism. J Neurochem 114:1414-1423, 2010.
49. Ongur D, Jensen JE, Prescot AP, Stork C, Lundy M, Cohen BM, Renshaw PF: Abnormal glutamatergic neurotransmission and neuronal-glial interactions in acute mania. Biol Psychiatry 64:718-726, 2008.
50. Page LA, Daly E, Schmitz N, Simmons A, Toal F, Deeley Q, Ambery F, McAlonan GM, Murphy KC, Murphy DG: In vivo 1H-magnetic resonance spectroscopy study of amygdala-hippocampal and parietal regions in autism. Am J Psychiatry 163:2189-2192, 2006.
51. Pereira FC, Rolo MR, Marques E, Mendes VM, Ribeiro CF, Ali SF, Morgadinho T, Macedo TR: Acute increase of the glutamate-glutamine cycling in discrete brain areas after administration of a single dose of amphetamine. Ann N Y Acad Sci 1139:212-221, 2008.
52. Perlov E, Philipsen A, Hesslinger B, Buechert M, Ahrendts J, Feige B, Bubl E, Hennig J, Ebert D, Tebartz van Elst L: Reduced cingulate glutamate/glutamine-to-creatine ratios in adult patients with attention deficit/hyperactivity disorder - a magnet resonance spectroscopy study. J Psychiatr Res 41:934-941, 2007.
53. Provencher SW: Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 14:260-264, 2001.
54. Provencher SW: Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30:672-679, 1993.
55. Purcell AE, Jeon OH, Zimmerman AW, Blue ME, Pevsner J: Postmortem brain abnormalities of the glutamate neurotransmitter system in autism. Neurology 57:1618-1628, 2001.
56. R Core Team: R: A Language and Environment for Statistical Computing. http://www. R-project.org/. Vienna, R Foundation for Statistical Computing, 2014.
57. Rojas DC, Singel D, Steinmetz S, Hepburn S, Brown MS: Decreased left perisylvian GABA concentration in children with autism and unaffected siblings. Neuroimage 86:28-34, 2014.
58. Schousboe A, Waagepetersen HS: Glial modulation of GABAergic and glutamatergic neurotransmission. Curr Top Med Chem 6:929-934, 2006.
59. Tarazi FI, Baldessarini RJ, Kula NS, Zhang K: Long-term effects of olanzapine, risperidone, and quetiapine on ionotropic glutamate receptor types: Implications for antipsychotic drug treatment. J Pharmacol Exp Ther 306:1145-1151, 2003.
60. Thakkar KN, Polli FE, Joseph RM, Tuch DS, Hadjikhani N, Barton JJ, Manoach DS: Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD). Brain 131:2464-2478, 2008.
61. Waddell KW, Avison MJ, Joers JM, Gore JC: A practical guide to robust detection of GABA in human brain by J-difference spectroscopy at 3 T using a standard volume coil. Magn Reson Imaging 25:1032-1038, 2007.
62. Wang L, Leslie DL: Health care expenditures for children with autism spectrum disorders in Medicaid. J Am Acad Child Adolesc Psychiatry 49:1165-1171, 2010.
63. Weschler D: Weschler Abbreviated Scale of Intelligence. San Antonio, NCS Pearson, 1999.
64. Wickham H: Ggplot2: Elegant graphics for data analysis. New York, Springer, 2009.
65. Yip J, Soghomonian JJ, Blatt GJ: Decreased GAD65 mRNA levels in select subpopulations of neurons in the cerebellar dentate nuclei in autism: An in situ hybridization study. Autism Res 2:50-59, 2009.
66. Yip J, Soghomonian JJ, Blatt GJ: Decreased GAD67 mRNA levels in cerebellar purkinje cells in autism: Pathophysiological implications. Acta Neuropathol 113:559-568, 2007.
67. Yuksel C, Ongur D: Magnetic resonance spectroscopy studies of glutamate-related abnormalities in mood disorders. Biol Psychiatry 68:785-794, 2010.
68. Zhu H, Edden RA, Ouwerkerk R, Barker PB: High resolution spectroscopic imaging of GABA at 3 tesla. Magn Reson Med 65:603-609, 2011.