Lowered frequency and impaired modulation of gamma band oscillations in a bimodal attention task are associated with reduced critical flicker frequency

NeuroImage

Volumn 61, Issue 1, 2012, Pages 216-227

  Kahlbrock, Nina ^a   Butz, Markus ^a,b   May, Elisabeth S ^a   Brenner, Meike ^a   Kircheis, Gerald ^a   Häussinger, Dieter ^a   Schnitzler, Alfons ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

CFF; GABA; Gamma; Hepatic encephalopathy; MEG; Oscillations

Indexed keywords

ARTICLE; ATTENTION DEFICIT DISORDER; BEHAVIORAL RESEARCH; BRAIN FUNCTION; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; CRITICAL FLICKER FUSION; DISEASE SEVERITY; GAMMA RHYTHM; HEPATIC ENCEPHALOPATHY; HUMAN; LIVER CIRRHOSIS; MAGNETOENCEPHALOGRAPHY; NEUROMODULATION; NEUROPATHOLOGY; PRIORITY JOURNAL; SYMPTOM; TASK PERFORMANCE; VISUAL STIMULATION;

ACOUSTIC STIMULATION; ADULT; AGED; ATTENTION; BEHAVIOR; DATA INTERPRETATION, STATISTICAL; ELECTROENCEPHALOGRAPHY; FEMALE; FLICKER FUSION; HEPATIC ENCEPHALOPATHY; HUMANS; INDIVIDUALITY; LIVER CIRRHOSIS; MAGNETOENCEPHALOGRAPHY; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; REACTION TIME;

EID: 84859077491     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.02.063     Document Type: Article

References (81)

1. Ahboucha S. Neurosteroids and hepatic encephalopathy: an update on possible pathophysiologic mechanisms. Curr. Mol. Pharmacol. 2011, 4(1):1-13.
2. Ahboucha S., Pomier-Layrargues G., Butterworth R.F. Increased brain concentrations of endogenous (non-benzodiazepine) GABA-A receptor ligands in human hepatic encephalopathy. Metab. Brain Dis. 2004, 19(3-4):241-251.
3. Amodio P., Gatta A. Neurophysiological investigation of hepatic encephalopathy. Metab. Brain Dis. 2005, 20(4):369-379.
4. Amodio P., Marchetti P., Del Piccolo F., Campo G., Rizzo C., Iemmolo R.M., Gerunda G., Caregaro L., Merkel C., Gatta A. Visual attention in cirrhotic patients: a study on covert visual attention orienting. Hepatology 1998, 27(6):1517-1523.
5. Amodio P., Marchetti P., Del Piccolo F., de Tourtchaninoff M., Varghese P., Zuliani C., Campo G., Gatta A., Guérit J.M. Spectral versus visual EEG analysis in mild hepatic encephalopathy. Clin. Neurophysiol. 1999, 110(8):1334-1344.
6. Amodio P., Schiff S., Del Piccolo F., Mapelli D., Gatta A., Umiltà C. Attention dysfunction in cirrhotic patients: an inquiry on the role of executive control, attention orienting and focusing. Metab. Brain Dis. 2005, 20(2):115-127.
7. Amodio P., Orsato R., Marchetti P., Schiff S., Poci C., Angeli P., Gatta A., Sparacino G., Toffolo G.M. Electroencephalographic analysis for the assessment of hepatic encephalopathy: comparison of non-parametric and parametric spectral estimation techniques. Neurophysiol. Clin./Clin. Neurophysiol. 2009, 39(2):107-115.
8. Amodio P., Ridola L., Schiff S., Montagnese S., Pasquale C., Nardelli S., Pentassuglio I., Trezza M., Marzano C., Flaiban C., Angeli P., Cona G., Bisiacchi P., Gatta A., Riggio O. Improving the inhibitory control task to detect minimal hepatic encephalopathy. Gastroenterology 2010, 139(2):510-518. 518.e1-2.
9. Bajaj J.S. Current and future diagnosis of hepatic encephalopathy. Metab. Brain Dis. 2010, 25(1):107-110.
10. Bassett M.L., Mullen K.D., Scholz B., Fenstermacher J.D., Jones E.A. Increased brain uptake of gamma-aminobutyric acid in a rabbit model of hepatic encephalopathy. Gastroenterology 1990, 98(3):747-757.
11. Butterworth R.F. Complications of cirrhosis III. Hepatic encephalopathy. J. Hepatol. 2000, 32(1 Suppl):171-180.
12. Butz M., Gross J., Timmermann L., Moll M., Freund H.-J., Witte O.W., Schnitzler A. Perilesional pathological oscillatory activity in the magnetoencephalogram of patients with cortical brain lesions. Neurosci. Lett. 2004, 355(1-2):93-96.
13. Conn H.O., Lieberthal M.M. Hepatic Coma; Lactulose; Disaccharides; Chemotherapy; Therapeutic Use; Drug Therapy 1979, Williams & Wilkins, Baltimore.
14. Davies M.G., Rowan M.J., Feely J. EEG and event related potentials in hepatic encephalopathy. Metab. Brain Dis. 1991, 6(4):175-186.
15. de Jongh A., Baayen J.C., de Munck J.C., Heethaar R.M., Vandertop W.P., Stam C.J. The influence of brain tumor treatment on pathological delta activity in MEG. Neuroimage 2003, 20(4):2291-2301.
16. Eberhardt G. Flimmerfrequenz-Analysator. Automatische Messmethode. Version 3.00. Dr. G. Schuhfried GmbH, Mödling, Austria 1994.
17. Engel A.K., Fries P. Beta-band oscillations - signalling the status quo?. Curr. Opin. Neurobiol. 2010, 20(2):156-165.
18. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291(5508):1560-1563.
19. Fries P., Scheeringa R., Oostenveld R. Finding gamma. Neuron 2008, 58(3):303-305.
20. Gaetz W., Edgar J.C., Wang D.J., Roberts T.P.L. Relating MEG measured motor cortical oscillations to resting γ-Aminobutyric acid (GABA) concentration. Neuroimage 2011, 55(2):616-621.
21. Gaetz W., Roberts T.P.L., Singh K.D., Muthukumaraswamy S.D. Functional and structural correlates of the aging brain: relating visual cortex (V1) gamma band responses to age-related structural change. Hum. Brain Mapp. 2011.
22. Gray C.M., König P., Engel A.K., Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 1989, 338(6213):334-337.
23. Green M.F. What are the functional consequences of neurocognitive deficits in schizophrenia?. Am. J. Psychiatry 1996, 153(3):321-330.
24. Green M.F., Mintz J., Salveson D., Nuechterlein K.H., Breitmeyer B., Light G.A., Braff D.L. Visual masking as a probe for abnormal gamma range activity in schizophrenia. Biol. Psychiatry 2003, 53(12):1113-1119.
25. Gross J., Kujala J., Hämäläinen M., Timmermann L., Schnitzler A., Salmelin R. Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(2):694-699.
26. Gruber T., Müller M.M., Keil A., Elbert T. Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clin. Neurophysiol. 1999, 110(12):2074-2085.
27. Guerit J.-M., Amantini A., Fischer C., Kaplan P.W., Mecarelli O., Schnitzler A., Ubiali E., Amodio P. Neurophysiological investigations of hepatic encephalopathy: ISHEN practice guidelines. Liver Int. 2009, 29(6):789-796.
28. Häussinger D., Schliess F. Pathogenetic mechanisms of hepatic encephalopathy. Gut 2008, 57(8):1156-1165.
29. Häussinger D., Kircheis G., Schliess F. Hepatic Encephalopathy and Nitrogen Metabolism 2006, Springer, Netherlands. 1st ed.
30. Herrmann C.S. Human EEG responses to 1-100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Exp. Brain Res. 2001, 137(3-4):346-353.
31. Holm S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 1979, 6(2):65-70.
32. Hoogenboom N., Schoffelen J.M., Oostenveld R., Parkes L.M., Fries P. Localizing human visual gamma-band activity in frequency, time and space. Neuroimage 2006, 29(3):764-773.
33. Hoogenboom N., Schoffelen J.M., Oostenveld R., Fries P. Visually induced gamma-band activity predicts speed of change detection in humans. Neuroimage 2010, 51(3):1162-1167.
34. Jones E.A., Schafer D.F., Ferenci P., Pappas S.C. The GABA hypothesis of the pathogenesis of hepatic encephalopathy: current status. Yale J. Biol. Med. 1984, 57(3):301-316.
35. Kahlbrock N., Butz M., May E.S., Schnitzler A. Sustained gamma band synchronization in early visual areas reflects the level of selective attention. Neuroimage 2012, 59(1):673-681.
36. Kaiser J., Hertrich I., Ackermann H., Lutzenberger W. Gamma-band activity over early sensory areas predicts detection of changes in audiovisual speech stimuli. Neuroimage 2006, 30(4):1376-1382.
37. Kircheis G., Wettstein M., Timmermann L., Schnitzler A., Häussinger D. Critical flicker frequency for quantification of low-grade hepatic encephalopathy. Hepatology 2002, 35(2):357-366.
38. Kircheis G., Fleig W.E., Görtelmeyer R., Grafe S., Häussinger D. Assessment of low-grade hepatic encephalopathy: a critical analysis. J. Hepatol. 2007, 47(5):642-650.
39. Kircheis G., Knoche A., Hilger N., Manhart F., Schnitzler A., Schulze H., Häussinger D. Hepatic encephalopathy and fitness to drive. Gastroenterology 2009, 137(5):1706-1715. e1-9.
40. Koenig T., Prichep L., Dierks T., Hubl D., Wahlund L.O., John E.R., Jelic V. Decreased EEG synchronization in Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging 2005, 26(2):165-171.
41. Kullmann F., Hollerbach S., Lock G., Holstege A., Dierks T., Schölmerich J. Brain electrical activity mapping of EEG for the diagnosis of (sub)clinical hepatic encephalopathy in chronic liver disease. Eur. J. Gastroenterol. Hepatol. 2001, 13(5):513-522.
42. Lachaux J.P., George N., Tallon-Baudry C., Martinerie J., Hugueville L., Minotti L., Kahane P., Renault B. The many faces of the gamma band response to complex visual stimuli. Neuroimage 2005, 25(2):491-501.
43. Marchetti P., D'Avanzo C., Orsato R., Montagnese S., Schiff S., Kaplan P.W., Piccione F., Merkel C., Gatta A., Sparacino G., Toffolo G.M., Amodio P. Electroencephalography in patients with cirrhosis. Gastroenterology 2011, 141(5):1680-1689. e1-2.
44. Maris E., Oostenveld R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 2007, 164(1):177-190.
45. Mattarozzi K., Campi C., Guarino M., Stracciari A. Distinguishing between clinical and minimal hepatic encephalopathy on the basis of specific cognitive impairment. Metab. Brain Dis. 2005, 20(3):243-249.
46. Montagnese S., Jackson C., Morgan M.Y. Spatio-temporal decomposition of the electroencephalogram in patients with cirrhosis. J. Hepatol. 2007, 46(3):447-458.
47. Montagnese S., Biancardi A., Schiff S., Carraro P., Carlà V., Mannaioni G., Moroni F., Tono N., Angeli P., Gatta A., Amodio P. Different biochemical correlates for different neuropsychiatric abnormalities in patients with cirrhosis. Hepatology 2011, 53(2):558-566.
48. Muthukumaraswamy S.D., Edden R.A.E., 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(20):8356-8361.
49. Muthukumaraswamy S.D., Singh K.D., Swettenham J.B., Jones D.K. Visual gamma oscillations and evoked responses: variability, repeatability and structural MRI correlates. Neuroimage 2010, 49(4):3349-3357.
50. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15(1):1-25.
51. Nolte G. The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. Phys. Med. Biol. 2003, 48(22):3637-3652.
52. Olesen S.S., Graversen C., Hansen T.M., Blauenfeldt R.A., Hansen J.B., Steimle K., Drewes A.M. Spectral and dynamic electroencephalogram abnormalities are correlated to psychometric test performance in hepatic encephalopathy. Scand. J. Gastroenterol. 2011, 46(7-8):988-996.
53. Oostenveld R., Fries P., Maris E., Schoffelen J.-M. FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 2011:156869.
54. Pantiga C., Rodrigo L.R., Cuesta M., Lopez L., Arias J.L. Cognitive deficits in patients with hepatic cirrhosis and in liver transplant recipients. J. Neuropsychiatry Clin. Neurosci. 2003, 15(1):84-89.
55. Parson-Smith B.G., Summerskill W.H., Dawson A.M., Sherlock S. The electroencephalograph in liver disease. Lancet 1957, 273(7001):867-871.
56. Prakash R., Mullen K.D. Mechanisms, diagnosis and management of hepatic encephalopathy. Nat. Rev. Gastroenterol. Hepatol. 2010, 7(9):515-525.
57. Pugh R.N.H., Murray-Lyon I.M., Dawson J.L., Pietroni M.C., Williams R. Transection of the oesophagus for bleeding oesophageal varices. Br. J. Surg. 1973, 60(8):646-649.
58. Rihs T.A., Michel C.M., Thut G. A bias for posterior α-band power suppression versus enhancement during shifting versus maintenance of spatial attention. Neuroimage 2009, 44(1):190-199.
59. Roelfsema P.R., Engel A.K., König P., Singer W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 1997, 385(6612):157-161.
60. Romero-Gómez M., Córdoba J., Jover R., del Olmo J.A., Ramírez M., Rey R., de Madaria E., Montoliu C., Nuñez D., Flavia M., Compañy L., Rodrigo J.M., Felipo V. Value of the critical flicker frequency in patients with minimal hepatic encephalopathy. Hepatology 2007, 45(4):879-885.
61. Schnitzler A., Gross J. Normal and pathological oscillatory communication in the brain. Nat. Rev. Neurosci. 2005, 6(4):285-296.
62. Sharma P., Sharma B.C., Puri V., Sarin S.K. Critical flicker frequency: diagnostic tool for minimal hepatic encephalopathy. J. Hepatol. 2007, 47(1):67-73.
63. Siegel M., Donner T.H., Oostenveld R., Fries P., Engel A.K. Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention. Neuron 2008, 60(4):709-719.
64. Spencer K.M., Nestor P.G., Perlmutter R., Niznikiewicz M.A., Klump M.C., Frumin M., Shenton M.E., McCarley R.W. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(49):17288-17293.
65. Starns J.J., Ratcliff R. The effects of aging on the speed-accuracy compromise: boundary optimality in the diffusion model. Psychol. Aging 2010, 25(2):377-390.
66. Steinmetz P.N., Roy A., Fitzgerald P.J., Hsiao S.S., Johnson K.O., Niebur E. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 2000, 404(6774):187-190.
67. Tallon-Baudry C., Bertrand O., Peronnet F., Pernier J. Induced gamma-band activity during the delay of a visual short-term memory task in humans. J. Neurosci. 1998, 18(11):4244-4254.
68. Tallon-Baudry C., Bertrand O., Henaff M.A., Isnard J., Fischer C. Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cereb. Cortex 2005, 15(5):654-662.
69. Thut G., Nietzel A., Brandt S.A., Pascual-Leone A. α-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J. Neurosci. 2006, 26(37):9494-9502.
70. Timmermann L., Gross J., Kircheis G., Häussinger D., Schnitzler A. Cortical origin of mini-asterixis in hepatic encephalopathy. Neurology 2002, 58(2):295-298.
71. Timmermann L., Gross J., Butz M., Kircheis G., Häussinger D., Schnitzler A. Mini-asterixis in hepatic encephalopathy induced by pathologic thalamo-motor-cortical coupling. Neurology 2003, 61(5):689-692.
72. Timmermann L., Butz M., Gross J., Kircheis G., Häussinger D., Schnitzler A. Neural synchronization in hepatic encephalopathy. Metab. Brain Dis. 2005, 20(4):337-346.
73. Timmermann L., Butz M., Gross J., Ploner M., Südmeyer M., Kircheis G., Häussinger D., Schnitzler A. Impaired cerebral oscillatory processing in hepatic encephalopathy. Clin. Neurophysiol. 2008, 119(2):265-272.
74. Uhlhaas P.J., Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 2006, 52(1):155-168.
75. Van der Rijt C.C., Schalm S.W., De Groot G.H., De Vlieger M. Objective measurement of hepatic encephalopathy by means of automated EEG analysis. Electroencephalogr. Clin. Neurophysiol. 1984, 57(5):423-426.
76. Vidal J.R., Chaumon M., O'Regan J.K., Tallon-Baudry C. Visual grouping and the focusing of attention induce gamma-band oscillations at different frequencies in human magnetoencephalogram signals. J. Cogn. Neurosci. 2006, 18(11):1850-1862.
77. Vienna test system, WINWTS, Version 4.50, 1999. Dr. G. Schuhfried GmbH. Mödling, Austria.
78. Weissenborn K., Heidenreich S., Ennen J., Rückert N., Hecker H. Attention deficits in minimal hepatic encephalopathy. Metab. Brain Dis. 2001, 16(1-2):13-19.
79. Weissenborn K., Heidenreich S., Giewekemeyer K., Rückert N., Hecker H. Memory function in early hepatic encephalopathy. J. Hepatol. 2003, 39(3):320-325.
80. Weissenborn K., Giewekemeyer K., Heidenreich S., Bokemeyer M., Berding G., Ahl B. Attention, memory, and cognitive function in hepatic encephalopathy. Metab. Brain Dis. 2005, 20(4):359-367.
81. Wyart V., Tallon-Baudry C. Neural dissociation between visual awareness and spatial attention. J. Neurosci. 2008, 28(10):2667-2679.