GABA in the insula - a predictor of the neural response to interoceptive awareness

NeuroImage

Volumn 86, Issue , 2014, Pages 10-18

  Wiebking, Christine ^a,b   Duncan, Niall W ^b   Tiret, Brice ^c   Hayes, Dave J ^b   Marjaǹska, Małgorzata ^d   Doyon, Julien ^c   Bajbouj, Malek ^a   Northoff, Georg ^b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b Clinical Epidemiology Program   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Depressed affect; FMRI; GABA; Insula; Interoception; MRS

Indexed keywords

4 AMINOBUTYRIC ACID;

4 AMINOBUTYRIC ACID BRAIN LEVEL; ADULT; AWARENESS; BECK HOPELESSNESS SCALE; BRAIN FUNCTION; EMOTIONAL DISORDER; EXTEROCEPTIVE AWARENESS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GABAERGIC SYSTEM; HUMAN; INSULA; INTEROCEPTIVE AWARENESS; MALE; NERVE POTENTIAL; NUCLEAR MAGNETIC RESONANCE IMAGING; PREDICTOR VARIABLE; PRIORITY JOURNAL; REVIEW; SENSORY STIMULATION; VOXEL BASED MORPHOMETRY; YOUNG ADULT; ANXIETY; ARTICLE; CONTROLLED STUDY; DEPRESSION; HEART BEAT; HUMAN EXPERIMENT; INTEROCEPTION; MENTAL DISEASE; MENTAL TASK; NOISE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROPRIOCEPTION; SIGNAL TRANSDUCTION; STIMULUS RESPONSE;

DEPRESSED AFFECT; FMRI; GABA; INSULA; INTEROCEPTION; MRS;

ADOLESCENT; ADULT; AWARENESS; BIOLOGICAL MARKERS; CEREBRAL CORTEX; FEMALE; GAMMA-AMINOBUTYRIC ACID; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEUROTRANSMITTER AGENTS; REFERENCE VALUES; SENSATION; TISSUE DISTRIBUTION; YOUNG ADULT;

EID: 84891625101     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.04.042     Document Type: Review

References (76)

1. Alcaro A., Panksepp J., Witczak J., Hayes D.J., Northoff G. Is subcortical-cortical midline activity in depression mediated by glutamate and GABA? A cross-species translational approach. Neurosci. Biobehav. Rev. 2010, 34:592-605.
2. Ashburner J., Friston K.J. Nonlinear spatial normalization using basis functions. Hum. Brain Mapp. 1999, 7:254-266.
3. Beck A.T., Weissman A., Lester D., Trexler L. The measurement of pessimism: the hopelessness scale. J. Consult. Clin. Psychol. 1974, 42:861-865.
4. Beck A.T., Steer R.A., Ball R., Ranieri W. Comparison of Beck Depression Inventories-IA and -II in psychiatric outpatients. J. Pers. Assess. 1996, 67:588-597.
5. Beckmann C.F., Smith S.M. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans. Med. Imaging 2004, 23:137-152.
6. Brett M., Anton J.L., Valabrgue R., Poline J.B. Region of interest analysis using an SPM toolbox. Presented at the 8th International Conference on Functional Mapping of the Human Brain, June 2-6, 2002, Sendai, Japan. Neuroimage 2002, 13:210-217.
7. Casey B.J., Cohen J.D., O'Craven K., Davidson R.J., Irwin W., Nelson C.A., Noll D.C., Hu X., Lowe M.J., Rosen B.R., Truwitt C.L., Turski P.A. Reproducibility of fMRI results across four institutions using a spatial working memory task. Neuroimage 1998, 8:249-261.
8. Cauda F., D'Agata F., Sacco K., Duca S., Geminiani G., Vercelli A. Functional connectivity of the insula in the resting brain. Neuroimage 2011, 55:8-23.
9. Chang L.J., Yarkoni T., Khaw M.W., Sanfey A.G. Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb. Cortex 2012, 23(3):739-749. 10.1093/cercor/bhs065.
10. Craig A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 2002, 3:655-666.
11. Craig A.D. How do you feel - now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10:59-70.
12. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nat. Neurosci. 2004, 7:189-195.
13. Croarkin P.E., Levinson A.J., Daskalakis Z.J. Evidence for GABAergic inhibitory deficits in major depressive disorder. Neurosci. Biobehav. Rev. 2011, 35:818-825.
14. Deen B., Pitskel N.B., Pelphrey K.A. Three systems of insular functional connectivity identified with cluster analysis. Cereb. Cortex (New York, N.Y.: 1991) 2011, 21:1498-1506.
15. Donahue M.J., Near J., Blicher J.U., Jezzard P. Baseline GABA concentration and fMRI response. Neuroimage 2010, 53:392-398.
16. Duncan N.W., Enzi B., Wiebking C., Northoff G. Involvement of glutamate in rest-stimulus interaction between perigenual and supragenual anterior cingulate cortex: a combined fMRI-MRS study. Hum. Brain Mapp. 2011, 32:2172-2182.
17. Dunn B.D., Galton H.C., Morgan R., Evans D., Oliver C., Meyer M., Cusack R., Lawrence A.D., Dalgleish T. Listening to your heart. How interoception shapes emotion experience and intuitive decision making. Psychol. Sci. 2010, 21:1835-1844.
18. Eickhoff S.B., Paus T., Caspers S., Grosbras M.-H., Evans A.C., Zilles K., Amunts K. Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 2007, 36:511-521.
19. Falkenberg L.E., Westerhausen R., Specht K., Hugdahl K. Resting-state glutamate level in the anterior cingulate predicts blood-oxygen level-dependent response to cognitive control. Proc. Natl. Acad. Sci. U. S. A. 2012, 1-6.
20. Farb N.A.S., Segal Z.V., Anderson A.K. Attentional modulation of primary interoceptive and exteroceptive cortices. Cereb. Cortex (New York, N.Y.: 1991) 2012, 1-13.
21. Friston K.J., Fletcher P., Josephs O., Holmes A., Rugg M.D., Turner R. Event-related fMRI: characterizing differential responses. Neuroimage 1998, 7:30-40.
22. 1H MRS of healthy human cortex, hippocampus, and thalamus: metabolite concentrations, quantification precision, and reproducibility. J. Magn. Reson. Imaging 2004, 20:366-371.
23. Gountouna V.E., Job D.E., McIntosh A.M., Moorhead T.W., Lymer G.K., Whalley H.C., Hall J., Waiter G.D., Brennan D., McGonigle D.J., Ahearn T.S., Cavanagh J., Condon B., Hadley D.M., Marshall I., Murray A.D., Steele J.D., Wardlaw J.M., Lawrie S.M. Functional magnetic resonance imaging (fMRI) reproducibility and variance components across visits and scanning sites with a finger tapping task. Neuroimage 2010, 49:552-560.
24. Grimm S., Beck J., Schuepbach D., Hell D., Boesiger P., Bermpohl F., Niehaus L., Boeker H., Northoff G. Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: an fMRI study in severe major depressive disorder. Biol. Psychiatry 2008, 63:369-376.
25. Grimm S., Ernst J., Boesiger P., Schuepbach D., Boeker H., Northoff G. Reduced negative BOLD responses in the default-mode network and increased self-focus in depression. World J. Biol. Psychiatry 2011, 12:627-637.
26. Gruetter R., Tkác I. Field mapping without reference scan using asymmetric echo-planar techniques. Magn. Reson. Med. 2000, 43:319-323.
27. Herbert B.M., Pollatos O., Schandry R. Interoceptive sensitivity and emotion processing: an EEG study. Int. J. Psychophysiol. 2007, 65:214-227.
28. Kaza E., Klose U., Lotze M. Comparison of a 32-channel with a 12-channel head coil: are there relevant improvements for functional imaging?. J. Magn. Reson. Imaging 2011, 34:173-183.
29. Kelly R.E., Alexopoulos G.S., Wang Z., Gunning F.M., Murphy C.F., Morimoto S.S., Kanellopoulos D., Jia Z., Lim K.O., Hoptman M.J. Visual inspection of independent components: defining a procedure for artifact removal from fMRI data. J. Neurosci. Methods 2010, 189:233-245.
30. Kelly C., Toro R., Di Martino A., Cox C.L., Bellec P., Castellanos F.X., Milham M.P. A convergent functional architecture of the insula emerges across imaging modalities. Neuroimage 2012, 61:1129-1142.
31. Kriegeskorte N., Simmons W.K., Bellgowan P.S., Baker C.I. Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 2009, 12:535-540.
32. Lamm C., Singer T. The role of anterior insular cortex in social emotions. Brain Struct. Funct. 2010, 214:579-591.
33. Liotti M., Mayberg H.S., McGinnis S., Brannan S.L., Jerabek P. Unmasking disease-specific cerebral blood flow abnormalities: mood challenge in patients with remitted unipolar depression. Am. J. Psychiatry 2002, 159:1830-1840.
34. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
35. Maldjian J.A., Laurienti P.J., Burdette J.H. Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 2004, 21:450-455.
36. Marjaǹska M., Henry P.G., Auerbach E.J., Franc D., Mueller B., Ugurbil K., Lim K.O. Reproducibility of in vivo GABA quantification in anterior cingulate at 3Tesla. Proc. Int. Soc. Magn. Reson. Med. 2007, 15.
37. McKeown M.J., Makeig S., Brown G.G., Jung T.P., Kindermann S.S., Bell A.J., Sejnowski T.J. Analysis of fMRI data by blind separation into independent spatial components. Hum. Brain Mapp. 1998, 6:160-188.
38. Mescher M., Merkle H., Kirsch J., Garwood M., Gruetter R. Simultaneous in vivo spectral editing and water suppression. NMR Biomed. 1998, 11:266-272.
39. Möhler H. The GABA system in anxiety and depression and its therapeutic potential. Neuropharmacology 2012, 62:42-53.
40. Muthukumaraswamy S.D., Edden R.A., Jones D.K., Swettenham J.B., Singh K.D. Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:8356-8361.
41. Muthukumaraswamy S.D., Evans C.J., Edden R.A.E., Wise R.G., Singh K.D. Individual variability in the shape and amplitude of the BOLD-HRF correlates with endogenous GABAergic inhibition. Hum. Brain Mapp. 2012, 33:455-465.
42. Northoff G., Walter M., Schulte R.F., Beck J., Dydak U., Henning A., Boeker H., Grimm S., Boesiger P. GABA concentrations in the human anterior cingulate cortex predict negative BOLD responses in fMRI. Nat. Neurosci. 2007, 10:1515-1517.
43. O'Gorman R.L., Michels L., Edden R.A., Murdoch J.B., Martin E. In vivo detection of GABA and glutamate with MEGA-PRESS: reproducibility and gender effects. J. Magn. Reson. Imaging 2011, 33:1262-1267.
44. Paulus M.P., Stein M.B. Interoception in anxiety and depression. Brain Struct. Funct. 2010, 214:451-463.
45. Poldrack R.A., Mumford J.A. Independence in ROI analysis: where is the voodoo?. Soc. Cogn. Affect. Neurosci. 2009, 4:208-213.
46. Pollatos O., Gramann K., Schandry R. Neural systems connecting interoceptive awareness and feelings. Hum. Brain Mapp. 2007, 28:9-18.
47. Pollatos O., Schandry R., Auer D.P., Kaufmann C. Brain structures mediating cardiovascular arousal and interoceptive awareness. Brain Res. 2007, 1141:178-187.
48. Price J.L., Drevets W.C. Neural circuits underlying the pathophysiology of mood disorders. Trends Cogn. Sci. 2012, 16:61-71.
49. Provencher S.W. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med. 1993, 30:672-679.
50. Provencher S.W. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed. 2001, 14:260-264.
51. Raichle M. A paradigm shift in functional brain imaging. J. Neurosci. 2009, 29:12729-12734.
52. Sanacora G., Treccani G., Popoli M. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 2012, 62:63-77.
53. Siegle G.J., Thompson W., Carter C.S., Steinhauer S.R., Thase M.E. Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol. Psychiatry 2007, 61:198-209.
54. Simmons W.K., Avery J.A., Barcalow J.C., Bodurka J., Drevets W.C., Bellgowan P. Keeping the body in mind: insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness. Hum. Brain Mapp. 2012, 000.
55. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23:S208-S219.
56. Sprengelmeyer R., Steele J.D., Mwangi B., Kumar P., Christmas D., Milders M., Matthews K. The insular cortex and the neuroanatomy of major depression. J. Affect. Disord. 2011, 133:120-127.
57. Stagg C.J., Best J.G., Stephenson M.C., O'Shea J., Wylezinska M., Kincses Z.T., Morris P.G., Matthews P.M., Johansen-Berg H. Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:5202-5206.
58. Stagg C.J., Bachtiar V., Johansen-Berg H. The role of GABA in human motor learning. Curr. Biol. 2011, 21:480-484.
59. Stagg C.J., Bestmann S., Constantinescu A.O., Moreno L.M., Allman C., Mekle R., Woolrich M., Near J., Johansen-Berg H., Rothwell J.C. Relationship between physiological measures of excitability and levels of glutamate and GABA in the human motor cortex. J. Physiol. 2011, 589:5845-5855.
60. Steiger J.H. Tests for comparing elements of a correlation matrix. Psychol. Bull. 1980, 87:245-251.
61. Sui J., Adali T., Pearlson G.D., Calhoun V.D. An ICA-based method for the identification of optimal FMRI features and components using combined group-discriminative techniques. Neuroimage 2009, 46:73-86.
62. Sumner P., Edden R.A.E., Bompas A., Evans C.J., Singh K.D. More GABA, less distraction: a neurochemical predictor of motor decision speed. Nat. Neurosci. 2010, 13:825-827.
63. Terasawa Y., Shibata M., Moriguchi Y., Umeda S. Anterior Insular Cortex Mediates Bodily Sensibility and Social Anxiety 2013.
64. Terhaar J., Viola F.C., Bär K.-J., Debener S. Heartbeat evoked potentials mirror altered body perception in depressed patients. Clin. Neurophysiol. 2012, 123:1950-1957.
65. 1H NMR spectroscopy of rat brain at 1ms echo time. Magn. Reson. Med. 1999, 41:649-656.
66. Vul E., Harris C., Winkielman P., Pashler H. Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition (a.k.a. voodoo correlations in social neuroscience). Perspect. Psychol. Sci. 2009, 4:274-290.
67. Wiebking C., Bauer A., De Greck M., Duncan N.W., Tempelmann C., Northoff G. Abnormal body perception and neural activity in the insula in depression: an fMRI study of the depressed "material me". World J. Biol. Psychiatry 2010, 11:538-549.
68. Wiebking C., De Greck M., Duncan N.W., Heinzel A., Tempelmann C., Northoff G. Are emotions associated with activity during rest or interoception? An exploratory fMRI study in healthy subjects. Neurosci. Lett. 2011, 491:87-92.
69. Wiebking C., Duncan N.W., Qin P., Hayes D.J., Lyttelton O., Gravel P., Verhaeghe J., Kostikov A.P., Schirrmacher R., Reader A.J., Bajbouj M., Northoff G. External awareness and GABA - a multimodal imaging study combining fMRI and [18F]flumazenil-PET. Hum. Brain Mapp. 2012, (Electronic publication ahead of print).
70. Wiens S. Interoception in emotional experience. Curr. Opin. Neurol. 2005, 18:442-447.
71. Williams E.J. The comparison of regression variables. J. R. Stat. Soc. 1959, 21:396-399.
72. Woolrich M., Jbabdi S., Patenaude B., Chappell M. Bayesian analysis of neuroimaging data in FSL. Neuroimage 2009, 45:S173-S186.
73. Zaki J., Davis J.I., Ochsner K.N. Overlapping activity in anterior insula during interoception and emotional experience. Neuroimage 2012, 62:493-499.
74. Zhao J., Bao A.-M., Qi X.-R., Kamphuis W., Luchetti S., Lou J.-S., Swaab D.F. Gene expression of GABA and glutamate pathway markers in the prefrontal cortex of non-suicidal elderly depressed patients. J. Affect. Disord. 2012, 138:494-502.
75. Zou K.H., Greve D.N., Wang M., Pieper S.D., Warfield S.K., White N.S., Manandhar S., Brown G.G., Vangel M.G., Kikinis R., Wells W.M. Reproducibility of functional MR imaging: preliminary results of prospective multi-institutional study performed by Biomedical Informatics Research Network. Radiology 2005, 237:781-789.
76. Zou Q., Wu C.W., Stein E.A., Zang Y., Yang Y. Static and dynamic characteristics of cerebral blood flow during the resting state. Neuroimage 2009, 48:515-524.