Multi-regional investigation of the relationship between functional MRI blood oxygenation level dependent (BOLD) activation and GABA concentration

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Harris, Ashley D ^a,b   Puts, Nicolaas A J ^a,b   Anderson, Brian A ^c   Yantis, Steven ^c   Pekar, James J ^a,b   Barker, Peter B ^a,b   Edden, Richard A E ^a,b  

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

^b KENNEDY KRIEGER INSTITUTE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; OXYGEN;

ADULT; ARTICLE; AUDITORY CORTEX; BOLD SIGNAL; BRAIN FUNCTION; COGNITION; CONTROLLED STUDY; CORRELATION COEFFICIENT; FEMALE; FINGER TAPPING TEST; FRONTAL EYE FIELD; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ACQUISITION; IMAGE ANALYSIS; MALE; MOTOR CONTROL; NOISE; NORMAL HUMAN; OCCIPITAL CORTEX; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; SACCADIC EYE MOVEMENT; SENSORIMOTOR CORTEX; SPATIAL MEMORY TEST; VISUAL STIMULATION; WORKING MEMORY; AUDITORY STIMULATION; BLOOD; BRAIN; BRAIN MAPPING; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY;

ACOUSTIC STIMULATION; ADULT; AUDITORY CORTEX; BRAIN; BRAIN MAPPING; FEMALE; GAMMA-AMINOBUTYRIC ACID; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; SENSORIMOTOR CORTEX;

EID: 84923833593     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117531     Document Type: Article

References (51)

1. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412: 150-157. PMID: 11449264
2. Wise RG, Harris AD, Stone AJ, Murphy K (2013) Measurement of OEF and absolute CMRO2: MRIbased methods using interleaved and combined hypercapnia and hyperoxia. Neuroimage 83: 135-147. doi: 10.1016/j.neuroimage.2013.06.008 PMID: 23769703
3. Lu H, Hua J, van Zijl PC (2013) Noninvasive functional imaging of cerebral blood volume with vascular-space- occupancy (VASO) MRI. NMR Biomed 26: 932-948. doi: 10.1002/nbm.2905 PMID: 23355392
4. Aguirre GK, Detre JA (2012) The development and future of perfusion fMRI for dynamic imaging of human brain activity. Neuroimage 62: 1279-1285. doi: 10.1016/j.neuroimage.2012.04.039 PMID: 22562056
5. Rae CD (2014) A guide to the metabolic pathways and function of metabolites observed in human brain (1)H magnetic resonance spectra. Neurochem Res 39: 1-36. doi: 10.1007/s11064-013-1199-5 PMID: 24258018
6. Rothman DL, Petroff OA, Behar KL, Mattson RH (1993) Localized 1H NMR measurements of gammaaminobutyric acid in human brain in vivo. Proc Natl Acad Sci U S A 90: 5662-5666. PMID: 8516315
7. Buzsaki G, Kaila K, Raichle M (2007) Inhibition and brain work. Neuron 56: 771-783. PMID: 18054855
8. Tagamets M-A, Horwitz B (2001) Interpreting PET and fMRI measures of functional neural activity: The effects of synaptic inhibition on cortical activation in human imaging studies. Brain Research Bulletin 54: 267-273. PMID: 11287131
9. Stagg CJ, Bachtiar V, Johansen-Berg H (2011) What are we measuring with GABA magnetic resonance spectroscopy? Commun Integr Biol 4: 573-575. doi: 10.4161/cib.4.5.16213 PMID: 22046466
10. Sanacora G, Mason GF, Rothman DL, Behar KL, Hyder F, et al. (1999) Reduced cortical gamma-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy. Arch Gen Psychiatry 56: 1043-1047. PMID: 10565505
11. Mullins PG, McGonigle DJ, O'Gorman RL, Puts NA, Vidyasagar R, et al. (2014) Current practice in the use of MEGA-PRESS spectroscopy for the detection of GABA. Neuroimage 86: 43-52. doi: 10.1016/j. neuroimage.2012.12.004 PMID: 23246994
12. Stagg CJ, Bachtiar V, Johansen-Berg H (2011) The role of GABA in human motor learning. Curr Biol 21: 480-484. doi: 10.1016/j.cub.2011.01.069 PMID: 21376596
13. Violante IR, Ribeiro MJ, Edden RA, Guimaraes P, Bernardino I, et al. (2013) GABA deficit in the visual cortex of patients with neurofibromatosis type 1: genotype-phenotype correlations and functional impact. Brain 136: 918-925. doi: 10.1093/brain/aws368 PMID: 23404336
14. Donahue MJ, Near J, Blicher JU, Jezzard P (2010) Baseline GABA concentration and fMRI response. Neuroimage 53: 392-398. doi: 10.1016/j.neuroimage.2010.07.017 PMID: 20633664
15. Muthukumaraswamy SD, Edden RA, Jones DK, Swettenham JB, Singh KD (2009) Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc Natl Acad Sci U S A 106: 8356-8361. doi: 10.1073/pnas.0900728106 PMID: 19416820
16. Muthukumaraswamy SD, Evans CJ, Edden RA, Wise RG, Singh KD (2012) Individual variability in the shape and amplitude of the BOLD-HRF correlates with endogenous GABAergic inhibition. Hum Brain Mapp 33: 455-465. doi: 10.1002/hbm.21223 PMID: 21416560
17. Northoff G, Walter M, Schulte RF, Beck J, Dydak U, et al. (2007) GABA concentrations in the human anterior cingulate cortex predict negative BOLD responses in fMRI. Nat Neurosci 10: 1515-1517.PMID: 17982452
18. Mescher M, Merkle H, Kirsch J, Garwood M, Gruetter R (1998) Simultaneous in vivo spectral editing and water suppression. NMR in Biomedicine 11: 266-272. PMID: 9802468
19. Tkac I, Starcuk Z, Choi IY, Gruetter R (1999) In vivo 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn Reson Med 41: 649-656. PMID: 10332839
20. Edden RAE, Puts NA, Harris AD, Barker PB, Evans CJ (2014) Gannet: a batch-processing tool for the quantitative analysis of GABA-edited MRS spectra. J Magn Reson Imaging In Press.
21. Near J, Edden R, Evans CJ, Paquin R, Harris A, et al. (2014) Frequency and phase drift correction of magnetic resonance spectroscopy data by spectral registration in the time domain. Magn Reson Med In Press.
22. Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20: 45-57. PMID: 11293691
23. Brainard DH (1997) The Psychophysics Toolbox. Spat Vis 10: 433-436. PMID: 9176952
24. Kleiner M, Brainard D, Pelli D. What's new in Psychtoolbox-3?; 2007; Perception, ECVP.
25. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17: 825-841. PMID: 12377157
26. Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17: 143-155. PMID: 12391568
27. Woolrich MW, Ripley BD, Brady M, Smith SM (2001) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14: 1370-1386. PMID: 11707093
28. Worsley KJ (2001) Statistical analysis of activation images. Ch 14. In: Jezzart P, Matthews PM, Smith SM, editors. Functional MRI: An Introduction to Methods: OUP.
29. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5: 143-156. PMID: 11516708
30. Wetzels R, Wagenmakers EJ (2012) A default Bayesian hypothesis test for correlations and partial correlations. Psychon Bull Rev 19: 1057-1064. doi: 10.3758/s13423-012-0295-x PMID: 22798023
31. Field AP, Gillett R (2010) How to do a meta-analysis. Br J Math Stat Psychol 63: 665-694. doi: 10. 1348/000711010X502733 PMID: 20497626
32. Button KS, Ioannidis JP, Mokrysz C, Nosek BA, Flint J, et al. (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14: 365-376. doi: 10.1038/nrn3475 PMID: 23571845
33. Epperson CN, O'Malley S, Czarkowski KA, Gueorguieva R, Jatlow P, et al. (2005) Sex, GABA, and nicotine: the impact of smoking on cortical GABA levels across the menstrual cycle as measured with proton magnetic resonance spectroscopy. Biol Psychiatry 57: 44-48. PMID: 15607299
34. Harada M, Kubo H, Nose A, Nishitani H, Matsuda T (2011) Measurement of variation in the human cerebral GABA level by in vivo MEGA-editing proton MR spectroscopy using a clinical 3 T instrument and its dependence on brain region and the female menstrual cycle. Hum Brain Mapp 32: 828-833. doi: 10. 1002/hbm.21086 PMID: 20645307
35. Epperson CN, Haga K, Mason GF, Sellers E, Gueorguieva R, et al. (2002) Cortical gamma-aminobutyric acid levels across the menstrual cycle in healthy women and those with premenstrual dysphoric disorder: a proton magnetic resonance spectroscopy study. Arch Gen Psychiatry 59: 851-858. PMID: 12215085
36. Donahue MJ, Rane S, Hussey E, Mason E, Pradhan S, et al. (2014) gamma-Aminobutyric acid (GABA) concentration inversely correlates with basal perfusion in human occipital lobe. J Cereb Blood Flow Metab.
37. Evans CJ, Puts NA, Robson SE, Boy F, McGonigle DJ, et al. (2012) Subtraction artifacts and frequency (Mis-)alignment in J-difference GABA editing. J Magn Reson Imaging.
38. Bogner W, Gruber S, Doelken M, Stadlbauer A, Ganslandt O, et al. (2010) In vivo quantification of intracerebral GABA by single-voxel (1)H-MRS-How reproducible are the results? Eur J Radiol 73: 526-531. doi: 10.1016/j.ejrad.2009.01.014 PMID: 19201120
39. Evans CJ, McGonigle DJ, Edden RA (2010) Diurnal stability of gamma-aminobutyric acid concentration in visual and sensorimotor cortex. J Magn Reson Imaging 31: 204-209. doi: 10.1002/jmri.21996 PMID: 20027589
40. O'Gorman RL, Michels L, Edden RA, Murdoch JB, Martin E (2011) In vivo detection of GABA and glutamate with MEGA-PRESS: reproducibility and gender effects. J Magn Reson Imaging 33: 1262-1267.doi: 10.1002/jmri.22520 PMID: 21509888
41. Harris AD, Glaubitz B, Near J, John Evans C, Puts NA, et al. (2013) Impact of frequency drift on gamma-aminobutyric acid-edited MR spectroscopy. Magn Reson Med In Press; doi: 10.1002/mrm. 25009.
42. Van Horn JD, Grafton ST, Miller MB (2008) Individual Variability in Brain Activity: A Nuisance or an Opportunity? Brain Imaging Behav 2: 327-334. PMID: 19777073
43. MacDonald SW, Nyberg L, Backman L (2006) Intra-individual variability in behavior: links to brain structure, neurotransmission and neuronal activity. Trends Neurosci 29: 474-480. PMID: 16820224
44. van Gelderen P, C WHW, de Zwart JA, Cohen L, Hallett M, et al. (2005) Resolution and reproducibility of BOLD and perfusion functional MRI at 3.0 Tesla. Magn Reson Med 54: 569-576. PMID: 16086372
45. Raemaekers M, du Plessis S, Ramsey NF, Weusten JM, Vink M (2012) Test-retest variability underlying fMRI measurements. Neuroimage 60: 717-727. doi: 10.1016/j.neuroimage.2011.11.061 PMID: 22155027
46. Gaxiola-Valdez I, Goodyear BG (2012) Origins of intersubject variability of blood oxygenation level dependent and arterial spin labeling fMRI: implications for quantification of brain activity. Magn Reson Imaging 30: 1394-1400. doi: 10.1016/j.mri.2012.05.002 PMID: 22795932
47. Terpstra M, Ugurbil K, Gruetter R (2002) Direct in vivo measurement of human cerebral GABA concentration using MEGA-editing at 7 Tesla. Magn Reson Med 47: 1009-1012. PMID: 11979581
48. Hetherington HP, Newcomer BR, Pan JW (1998) Measurements of human cerebral GABA at 4.1 T using numerically optimized editing pulses. Magn Reson Med 39: 6-10. PMID: 9438430
49. Edden RA, Puts NA, Barker PB (2012) Macromolecule-suppressed GABA-edited magnetic resonance spectroscopy at 3T. Magn Reson Med 68: 657-661. doi: 10.1002/mrm.24391 PMID: 22777748
50. Henry P-G, Dautry C, Hantraye P, Bloch G (2001) Brain GABA editing without macromolecule contamination. Magn Reson Med 45: 517-520. PMID: 11241712
51. Near J, Simpson R, Cowen P, Jezzard P (2011) Efficient gamma-aminobutyric acid editing at 3T without macromolecule contamination: MEGA-SPECIAL. NMR Biomed 24: 1277-1285. doi: 10.1002/nbm.1688 PMID: 21387450