Abnormal relationship between GABA, neurophysiology and impulsive behavior in neurofibromatosis type 1

Cortex

Volumn 64, Issue , 2015, Pages 194-208

  Ribeiro, Maria J ^a   Violante, Inês R ^a   Bernardino, Inês ^a   Edden, Richard A E ^b,c   Castelo Branco, Miguel ^a  

^a UNIVERSITY OF COIMBRA   (Portugal)

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

^c KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

Electroencephalography; Gamma aminobutyric acid; Impulse control disorders; Magnetic resonance spectroscopy; Neurofibromatosis type 1; Prefrontal cortex

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; NEUROTRANSMITTER; GLUTAMINE;

ACTION POTENTIAL; ADOLESCENT; AGE DISTRIBUTION; ARTICLE; BEHAVIOR CONTROL; BRAIN FUNCTION; BRAIN REGION; CHILD; CLINICAL ARTICLE; CLINICAL ASSESSMENT; COGNITION; COMPARATIVE STUDY; CONTROL; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; EVOKED RESPONSE; FEMALE; FRONTAL CORTEX; GABAERGIC SYSTEM; HUMAN; IMPULSE CONTROL DISORDER; IMPULSIVENESS; INTELLIGENCE; MALE; NEUROFIBROMATOSIS; NEUROFIBROMATOSIS TYPE 1; NEUROPHYSIOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OCCIPITAL CORTEX; PERFORMANCE; TASK PERFORMANCE; ATTENTION; BRAIN; EXECUTIVE FUNCTION; INHIBITION (PSYCHOLOGY); METABOLISM; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; YOUNG ADULT;

ADOLESCENT; ATTENTION; BRAIN; CHILD; ELECTROENCEPHALOGRAPHY; EXECUTIVE FUNCTION; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLUTAMINE; HUMANS; IMPULSIVE BEHAVIOR; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEUROFIBROMATOSIS 1; NEUROPSYCHOLOGICAL TESTS; YOUNG ADULT;

EID: 84912098947     PISSN: 00109452     EISSN: 19738102     Source Type: Journal    
DOI: 10.1016/j.cortex.2014.10.019     Document Type: Article

References (91)

1. Aron A.R. From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biological Psychiatry 2011, 69(12):e55-68.
2. Billingsley R.L., Jackson E.F., Slopis J.M., Swank P.R., Mahankali S., Moore B.D. Functional MRI of visual-spatial processing in neurofibromatosis, type I. Neuropsychologia 2004, 42(3):395-404.
3. Bogner W., Gruber S., Doelken M., Stadlbauer A., Ganslandt O., Boettcher U., et al. Invivo quantification of intracerebral GABA by single-voxel (1)H-MRS-How reproducible are the results?. European Journal of Radiology 2010, 73(3):526-531.
4. Boy F., Evans C.J., Edden R.A., Lawrence A.D., Singh K.D., Husain M., et al. Dorsolateral prefrontal gamma-aminobutyric acid in men predicts individual differences in rash impulsivity. Biological Psychiatry 2011, 70(9):866-872.
5. Boy F., Evans C.J., Edden R.A., Singh K.D., Husain M., Sumner P. Individual differences in subconscious motor control predicted by GABA concentration in SMA. Current Biology 2010, 20(19):1779-1785.
6. Brainard D.H. The psychophysics toolbox. Spatial Vision 1997, 10(4):433-436.
7. Bruin K.J., Wijers A.A. Inhibition, response mode, and stimulus probability: a comparative event-related potential study. Clinical Neurophysiology 2002, 113(7):1172-1182.
8. Chen C.Y., Muggleton N.G., Tzeng O.J., Hung D.L., Juan C.H. Control of prepotent responses by the superior medial frontal cortex. NeuroImage 2009, 44(2):537-545.
9. Clements-Stephens A.M., Rimrodt S.L., Gaur P., Cutting L.E. Visuospatial processing in children with neurofibromatosis type 1. Neuropsychologia 2008, 46(2):690-697.
10. Codispoti M., Ferrari V., Junghofer M., Schupp H.T. The categorization of natural scenes: brain attention networks revealed by dense sensor ERPs. NeuroImage 2006, 32(2):583-591.
11. Conners C.K., Epstein J.N., Angold A., Klaric J. Continuous performance test performance in a normative epidemiological sample. Journal of Abnormal Child Psychology 2003, 31(5):555-562.
12. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience 2002, 3(3):201-215.
13. Costa R.M., Federov N.B., Kogan J.H., Murphy G.G., Stern J., Ohno M., et al. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 2002, 415(6871):526-530.
14. Cui Y., Costa R.M., Murphy G.G., Elgersma Y., Zhu Y., Gutmann D.H., et al. Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 2008, 135(3):549-560.
15. Descheemaeker M.J., Ghesquiere P., Symons H., Fryns J.P., Legius E. Behavioural, academic and neuropsychological profile of normally gifted Neurofibromatosis type 1 children. Journal of Intellectual Disability Research 2005, 49(Pt 1):33-46.
16. Diamond A. Executive functions. Annual Review of Psychology 2013, 64:135-168.
17. Dimoska A., Johnstone S.J., Barry R.J. The auditory-evoked N2 and P3 components in the stop-signal task: indices of inhibition, response-conflict or error-detection?. Brain and Cognition 2006, 62(2):98-112.
18. van Dinteren R., Arns M., Jongsma M.L., Kessels R.P. P300 development across the lifespan: a systematic review and meta-analysis. PLoS One 2014, 9(2):e87347.
19. Dockree P.M., Kelly S.P., Robertson I.H., Reilly R.B., Foxe J.J. Neurophysiological markers of alert responding during goal-directed behavior: a high-density electrical mapping study. NeuroImage 2005, 27(3):587-601.
20. Duarte J.V., Ribeiro M.J., Violante I.R., Cunha G., Silva E., Castelo-Branco M. Multivariate pattern analysis reveals subtle brain anomalies relevant to the cognitive phenotype in neurofibromatosis type 1. Human Brain Mapping 2014, 35(1):89-106.
21. Edden R.A., Barker P.B. Spatial effects in the detection of gamma-aminobutyric acid: improved sensitivity at high fields using inner volume saturation. Magnetic Resonance in Medicine 2007, 58(6):1276-1282.
22. Edden R.A., Crocetti D., Zhu H., Gilbert D.L., Mostofsky S.H. Reduced GABA concentration in attention-deficit/hyperactivity disorder. Archives of General Psychiatry 2012, 69(7):750-753.
23. Edden R.A., Muthukumaraswamy S.D., Freeman T.C., Singh K.D. Orientation discrimination performance is predicted by GABA concentration and gamma oscillation frequency in human primary visual cortex. Journal of Neuroscience 2009, 29(50):15721-15726.
24. Edden R.A., Puts N.A.J., Harris A.D., Barker P.B., Evans C.J. Gannet: a batch-processing tool for the quantitative analysis of gamma-aminobutyric acid - edited MR spectroscopy spectra. Journal of Magnetic Resonance Imaging 2014, 40:1445-1452.
25. Epstein J.N., Erkanli A., Conners C.K., Klaric J., Costello J.E., Angold A. Relations between Continuous Performance Test performance measures and ADHD behaviors. Journal of Abnormal Child Psychology 2003, 31(5):543-554.
26. Falkenstein M., Hoormann J., Hohnsbein J. ERP components in Go/Nogo tasks and their relation to inhibition. Acta Psychologica (Amsterdam) 1999, 101(2-3):267-291.
27. Fallgatter A.J., Ehlis A.C., Seifert J., Strik W.K., Scheuerpflug P., Zillessen K.E., et al. Altered response control and anterior cingulate function in attention-deficit/hyperactivity disorder boys. Clinical Neurophysiology 2004, 115(4):973-981.
28. Ferner R.E., Hughes R.A., Weinman J. Intellectual impairment in neurofibromatosis 1. Journal of the Neurological Sciences 1996, 138(1-2):125-133.
29. Gaetz W., Bloy L., Wang D.J., Port R.G., Blaskey L., Levy S.E., et al. GABA estimation in the brains of children on the autism spectrum: measurement precision and regional cortical variation. NeuroImage 2014, 86:1-9.
30. Gao F., Edden R.A., Li M., Puts N.A., Wang G., Liu C., et al. Edited magnetic resonance spectroscopy detects an age-related decline in brain GABA levels. NeuroImage 2013, 78:75-82.
31. Gilboa Y., Rosenblum S., Fattal-Valevski A., Toledano-Alhadef H., Rizzo A.S., Josman N. Using a virtual classroom environment to describe the attention deficits profile of children with neurofibromatosis type 1. Research in Developmental Disabilities 2011, 32(6):2608-2613.
32. Goddard A.W., Mason G.F., Appel M., Rothman D.L., Gueorguieva R., Behar K.L., et al. Impaired GABA neuronal response to acute benzodiazepine administration in panic disorder. American Journal of Psychiatry 2004, 161(12):2186-2193.
33. Golan H., Talpalar A.E., Schleifstein-Attias D., Grossman Y. GABA metabolism controls inhibition efficacy in the mammalian CNS. Neuroscience Letters 1996, 217(1):25-28.
34. Goldstein A., Spencer K.M., Donchin E. The influence of stimulus deviance and novelty on the P300 and novelty P3. Psychophysiology 2002, 39(6):781-790.
35. Gomez R., Behar K.L., Watzl J., Weinzimer S.A., Gulanski B., Sanacora G., et al. Intravenous ethanol infusion decreases human cortical gamma-aminobutyric acid and N-acetylaspartate as measured with proton magnetic resonance spectroscopy at 4 tesla. Biological Psychiatry 2012, 71(3):239-246.
36. Groom M.J., Scerif G., Liddle P.F., Batty M.J., Liddle E.B., Roberts K.L., et al. Effects of motivation and medication on electrophysiological markers of response inhibition in children with attention-deficit/hyperactivity disorder. Biological Psychiatry 2010, 67(7):624-631.
37. Hart H., Radua J., Nakao T., Mataix-Cols D., Rubia K. Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry 2013, 70(2):185-198.
38. Hillyard S.A., Anllo-Vento L. Event-related brain potentials in the study of visual selective attention. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(3):781-787.
39. Huijbregts S., Swaab H., de Sonneville L. Cognitive and motor control in neurofibromatosis type I: influence of maturation and hyperactivity-inattention. Developmental Neuropsychology 2010, 35(6):737-751.
40. Huijbregts S.C., de Sonneville L.M. Does cognitive impairment explain behavioral and social problems of children with neurofibromatosis type 1?. Behavior Genetics 2011, 41(3):430-436.
41. Huster R.J., Enriquez-Geppert S., Lavallee C.F., Falkenstein M., Herrmann C.S. Electroencephalography of response inhibition tasks: functional networks and cognitive contributions. International Journal of Psychophysiology 2013, 87(3):217-233.
42. Huster R.J., Westerhausen R., Pantev C., Konrad C. The role of the cingulate cortex as neural generator of the N200 and P300 in a tactile response inhibition task. Human Brain Mapping 2010, 31(8):1260-1271.
43. Hyman S.L., Shores A., North K.N. The nature and frequency of cognitive deficits in children with neurofibromatosis type 1. Neurology 2005, 65(7):1037-1044.
44. Jahfari S., Waldorp L., van den Wildenberg W.P., Scholte H.S., Ridderinkhof K.R., Forstmann B.U. Effective connectivity reveals important roles for both the hyperdirect (fronto-subthalamic) and the indirect (fronto-striatal-pallidal) fronto-basal ganglia pathways during response inhibition. Journal of Neuroscience 2011, 31(18):6891-6899.
45. Jensen J.E., Frederick Bde B., Renshaw P.F. Grey and white matter GABA level differences in the human brain using two-dimensional, J-resolved spectroscopic imaging. NMR in Biomedicine 2005, 18(8):570-576.
46. Karlsgodt K.H., Rosser T., Lutkenhoff E.S., Cannon T.D., Silva A., Bearden C.E. Alterations in white matter microstructure in neurofibromatosis-1. PLoS One 2012, 7(10):e47854.
47. Kok A. On the utility of P3 amplitude as a measure of processing capacity. Psychophysiology 2001, 38(3):557-577.
48. Levine T.M., Materek A., Abel J., O'Donnell M., Cutting L.E. Cognitive profile of neurofibromatosis type 1. Seminars in Pediatric Neurology 2006, 13(1):8-20.
49. Li W., Cui Y., Kushner S.A., Brown R.A., Jentsch J.D., Frankland P.W., et al. The HMG-CoA reductase inhibitor lovastatin reverses the learning and attention deficits in a mouse model of neurofibromatosis type 1. Current Biology 2005, 15(21):1961-1967.
50. Long Z., Medlock C., Dzemidzic M., Shin Y.W., Goddard A.W., Dydak U. Decreased GABA levels in anterior cingulate cortex/medial prefrontal cortex in panic disorder. Progress In Neuro-Psychopharmacology & Biological Psychiatry 2013, 44C:131-135.
51. Mescher M., Merkle H., Kirsch J., Garwood M., Gruetter R. Simultaneous invivo spectral editing and water suppression. NMR in Biomedicine 1998, 11(6):266-272.
52. Naatanen R., Kujala T., Winkler I. Auditory processing that leads to conscious perception: a unique window to central auditory processing opened by the mismatch negativity and related responses. Psychophysiology 2011, 48(1):4-22.
53. Nicita F., Di Biasi C., Sollaku S., Cecchini S., Salpietro V., Pittalis A., et al. Evaluation of the basal ganglia in neurofibromatosis type 1. Child's Nervous System 2014, 30(2):319-325.
54. Nieuwenhuis S., Yeung N., Cohen J.D. Stimulus modality, perceptual overlap, and the go/no-go N2. Psychophysiology 2004, 41(1):157-160.
55. Nieuwenhuis S., Yeung N., van den Wildenberg W., Ridderinkhof K.R. Electrophysiological correlates of anterior cingulate function in a go/no-go task: effects of response conflict and trial type frequency. Cognitive, Affective, & Behavioral Neuroscience 2003, 3(1):17-26.
56. NIH Neurofibromatosis conference statement, national institutes of health consensus development conference 1988, From. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve%26db=PubMed%26dopt=Citation%26list_uids=3128965.
57. Obeso I., Robles N., Marron E.M., Redolar-Ripoll D. Dissociating the role of the pre-SMA in response inhibition and switching: a combined online and offline TMS approach. Frontiers in Human Neuroscience 2013, 7:150.
58. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9(1):97-113.
59. Ouyang G., Schacht A., Zhou C., Sommer W. Overcoming limitations of the ERP method with Residue Iteration Decomposition (RIDE): a demonstration in go/no-go experiments. Psychophysiology 2013, 50(3):253-265.
60. Ozonoff S. Cognitive impairment in neurofibromatosis type 1. American Journal of Medical Genetics 1999, 89(1):45-52.
61. Payne J.M., Moharir M.D., Webster R., North K.N. Brain structure and function in neurofibromatosis type 1: current concepts and future directions. Journal of Neurology Neurosurgery and Psychiatry 2010, 81(3):304-309.
62. Perrin F., Pernier J., Bertrand O., Echallier J.F. Spherical splines for scalp potential and current density mapping. Electroencephalography and Clinical Neurophysiology 1989, 72(2):184-187.
63. Picton T.W., Stuss D.T., Alexander M.P., Shallice T., Binns M.A., Gillingham S. Effects of focal frontal lesions on response inhibition. Cerebral Cortex 2007, 17(4):826-838.
64. Polich J. Updating P300: an integrative theory of P3a and P3b. Clinical Neurophysiology 2007, 118(10):2128-2148.
65. Puts N.A., Edden R.A., Evans C.J., McGlone F., McGonigle D.J. Regionally specific human GABA concentration correlates with tactile discrimination thresholds. Journal of Neuroscience 2011, 31(46):16556-16560.
66. Quetscher C., Yildiz A., Dharmadhikari S., Glaubitz B., Schmidt-Wilcke T., Dydak U., et al. Striatal GABA-MRS predicts response inhibition performance and its cortical electrophysiological correlates. Brain Structure & Function 2014, [Epub ahead of print].
67. Ribeiro M.J., Violante I.R., Bernardino I., Ramos F., Saraiva J., Reviriego P., et al. Abnormal achromatic and chromatic contrast sensitivity in neurofibromatosis type 1. Investigative Ophthalmology & Visual Science 2012, 53(1):287-293.
68. Rojas D.C., Singel D., Steinmetz S., Hepburn S., Brown M.S. Decreased left perisylvian GABA concentration in children with autism and unaffected siblings. NeuroImage 2014, 86:28-34.
69. Rothman D.L., Behar K.L., Prichard J.W., Petroff O.A. Homocarnosine and the measurement of neuronal pH in patients with epilepsy. Magnetic Resonance in Medicine 1997, 38(6):924-929.
70. Rowbotham I., Pit-ten Cate I.M., Sonuga-Barke E.J., Huijbregts S.C. Cognitive control in adolescents with neurofibromatosis type 1. Neuropsychology 2009, 23(1):50-60.
71. Rubia K., Russell T., Overmeyer S., Brammer M.J., Bullmore E.T., Sharma T., et al. Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. NeuroImage 2001, 13(2):250-261.
72. Shilyansky C., Karlsgodt K.H., Cummings D.M., Sidiropoulou K., Hardt M., James A.S., et al. Neurofibromin regulates corticostriatal inhibitory networks during working memory performance. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(29):13141-13146.
73. Silveri M.M., Sneider J.T., Crowley D.J., Covell M.J., Acharya D., Rosso I.M., et al. Frontal lobe gamma-aminobutyric acid levels during adolescence: associations with impulsivity and response inhibition. Biological Psychiatry 2013, 74(4):296-304.
74. Simmonds D.J., Pekar J.J., Mostofsky S.H. Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 2008, 46(1):224-232.
75. Smigielska-Kuzia J., Bockowski L., Sobaniec W., Kulak W., Sendrowski K. Amino acid metabolic processes in the temporal lobes assessed by proton magnetic resonance spectroscopy (1H MRS) in children with Down syndrome. Pharmacological Reports 2010, 62(6):1070-1077.
76. Smith J.L., Jamadar S., Provost A.L., Michie P.T. Motor and non-motor inhibition in the Go/NoGo task: an ERP and fMRI study. International Journal of Psychophysiology 2013, 87(3):244-253.
77. Smith J.L., Johnstone S.J., Barry R.J. Movement-related potentials in the Go/NoGo task: the P3 reflects both cognitive and motor inhibition. Clinical Neurophysiology 2008, 119(3):704-714.
78. Smith J.L., Smith E.A., Provost A.L., Heathcote A. Sequence effects support the conflict theory of N2 and P3 in the Go/NoGo task. International Journal of Psychophysiology 2010, 75(3):217-226.
79. Sumner P., Edden R.A., Bompas A., Evans C.J., Singh K.D. More GABA, less distraction: a neurochemical predictor of motor decision speed. Nature Neuroscience 2010, 13(7):825-827.
80. Tonsgard J.H. Clinical manifestations and management of neurofibromatosis type 1. Seminars in Pediatric Neurology 2006, 13(1):2-7.
81. Violante I.R., Ribeiro M.J., Cunha G., Bernardino I., Duarte J.V., Ramos F., et al. Abnormal brain activation in neurofibromatosis type 1: a link between visual processing and the default mode network. PLoS One 2012, 7(6):e38785.
82. Violante I.R., Ribeiro M.J., Edden R.A., Guimaraes P., Bernardino I., Rebola J., et al. GABA deficit in the visual cortex of patients with neurofibromatosis type 1: genotype-phenotype correlations and functional impact. Brain 2013, 136(Pt 3):918-925.
83. Violante I.R., Ribeiro M.J., Silva E.D., Castelo-Branco M. Gyrification, cortical and subcortical morphometry in neurofibromatosis type 1: an uneven profile of developmental abnormalities. Journal of Neurodevelopmental Disorders 2013, 5(1):3.
84. Vogel E.K., Luck S.J. The visual N1 component as an index of a discrimination process. Psychophysiology 2000, 37(2):190-203.
85. Wechsler D. Manual for intelligence scale for children 2003, Cegoc-Tea, Lisbon.
86. Wechsler D. Manual for intelligence scale for adults 2008, Cegoc-Tea, Lisbon.
87. Wiersema J.R., Roeyers H. ERP correlates of effortful control in children with varying levels of ADHD symptoms. Journal of Abnormal Child Psychology 2009, 37(3):327-336.
88. Wylie G.R., Javitt D.C., Foxe J.J. Task switching: a high-density electrical mapping study. NeuroImage 2003, 20(4):2322-2342.
89. Yoon J.H., Maddock R.J., Rokem A., Silver M.A., Minzenberg M.J., Ragland J.D., et al. GABA concentration is reduced in visual cortex in schizophrenia and correlates with orientation-specific surround suppression. Journal of Neuroscience 2010, 30(10):3777-3781.
90. Yordanova J., Kolev V., Hohnsbein J., Falkenstein M. Sensorimotor slowing with ageing is mediated by a functional dysregulation of motor-generation processes: evidence from high-resolution event-related potentials. Brain 2004, 127(Pt 2):351-362.
91. Zhang W., Luck S.J. Feature-based attention modulates feedforward visual processing. Nature Neuroscience 2009, 12(1):24-25.