Early- and late-latency gamma auditory steady-state response in schizophrenia during closed eyes: Does hallucination status matter?

Clinical Neurophysiology

Volumn 127, Issue 5, 2016, Pages 2214-2221

  Griskova Bulanova, Inga ^a,b   Hubl, Daniela ^c   van Swam, Claudia ^c   Dierks, Thomas ^c   Koenig, Thomas ^c  

^a VILNIUS UNIVERSITY   (Lithuania)

^b Republican Vilnius Psychiatric Hospital   (Lithuania)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

Auditory steady state response; Gamma activity; Hallucinations; Schizophrenia

Indexed keywords

ADULT; ARTICLE; AUDITORY HALLUCINATION; AUDITORY RESPONSE; AUDITORY STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; LATENT PERIOD; MENTAL DISEASE; NEGATIVE SYNDROME; POSITIVE AND NEGATIVE SYNDROME SCALE; POSITIVE SYNDROME; PREVALENCE; PRIORITY JOURNAL; SCHIZOPHRENIA; SENSORY STIMULATION; STEADY STATE; AUDITORY EVOKED POTENTIAL; BRAIN; BRAIN MAPPING; ELECTROENCEPHALOGRAPHY; FEMALE; HALLUCINATION; MALE; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADULT; BRAIN; BRAIN MAPPING; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; FEMALE; HALLUCINATIONS; HUMANS; MALE; MIDDLE AGED; SCHIZOPHRENIA;

EID: 84960468411     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2016.02.009     Document Type: Article

References (64)

1. Angelopoulos E., Koutsoukos E., Maillis A., Papadimitriou G.N., Stefanis C. Cortical interactions during the experience of auditory verbal hallucinations. J Neuropsychiatry Clin Neurosci 2011, 23(3):287-293.
2. Arnfred S.M., Hansen L.K., Parnas J., Mørup M. Regularity increases middle latency evoked and late induced beta brain response following proprioceptive stimulation. Brain Res 2008, 1218:114-131.
3. Arnfred S.M., Raballo A., Morup M., Parnas J. Self-disorder and brain processing of proprioception in schizophrenia spectrum patients: a re-analysis. Psychopathology 2015, 48(1):60-64.
4. Brenner C.A., Krishnan G.P., Vohs J.L., Ahn W.Y., Hetrick W.P., Morzorati S.L., O'Donnell B.F. Steady state responses: electrophysiological assessment of sensory function in schizophrenia. Schizophr Bull 2009, 35(6):1065-1077.
5. Chang X., Xi Y.B., Cui L.B., Wang H.N., Sun J.B., Zhu Y.Q., Huang P., Collin G., Liu K., Xi M., Qi S., Tan Q.R., Miao D.M., Yin H. Distinct inter-hemispheric dysconnectivity in schizophrenia patients with and without auditory verbal hallucinations. Sci Rep 2015, 5:11218.
6. Cohen L.T., Rickards F.W., Clark G.M. A comparison of steady-state evoked potentials to modulated tones in awake and sleeping humans. J Acoust Soc Am 1991, 90(5):2467-2479.
7. Delorme A., Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 2004, 134(1):9-21.
8. Delorme A., Sejnowski T., Makeig S. Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis. Neuroimage 2007, 34(4):1443-1449.
9. Dierks T., Linden D.E., Jandl M., Formisano E., Goebel R., Lanfermann H., Singer W. Activation of Heschl's gyrus during auditory hallucinations. Neuron 1999, 22(3):615-621.
10. Eckhorn R., Bauer R., Jordan W., Brosch M., Kruse W., Munk M., Reitboeck H.J. Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol Cybern 1988, 60(2):121-130.
11. Gander P.E., Bosnyak D.J., Roberts L.E. Evidence for modality-specific but not frequency-specific modulation of human primary auditory cortex by attention. Hear Res 2010, 268(1-2):213-226.
12. Griskova I., Morup M., Parnas J., Ruksenas O., Arnfred S.M. The amplitude and phase precision of 40 Hz auditory steady-state response depend on the level of arousal. Exp Brain Res 2007, 183(1):133-138.
13. Griskova-Bulanova I., Dapsys K., Maciulis V., Arnfred S.M. Closed eyes condition increases auditory brain responses in schizophrenia. Psychiatry Res Neuroimaging 2013, 211(2):183-185.
14. Griskova-Bulanova I., Morup M., Parnas J., Ruksenas O., Arnfred S.M. Two discrete components of the 20 Hz steady-state response are distinguished through the modulation of activation level. Clin Neurophysiol 2009, 120(5):904-909.
15. Griskova I., Ruksenas O., Dapsys K., Maciulis V., Arnfred S.M.H. Distraction task rather than focal attention modulates gamma activity associated with auditory steady-state responses (ASSRs). Clin Neurophysiol 2011, 122(8):1541-1548.
16. Hamm J.P., Gilmore C.S., Picchetti N.A., Sponheim S.R., Clementz B.A. Abnormalities of neuronal oscillations and temporal integration to low- and high-frequency auditory stimulation in schizophrenia. Biol Psychiatry 2011, 69(10):989-996.
17. Herdman A.T., Lins O., Van Roon P., Stapells D.R., Scherg M., Picton T.W. Intracerebral sources of human auditory steady-state responses. Brain Topography 2002, 15(2):69-86.
18. Hirano Y., Oribe N., Kanba S., Onitsuka T., Nestor P.G., Spencer K.M. Spontaneous gamma activity in schizophrenia. JAMA Psychiatry 2015, 72(8):813-821.
19. Hong L.E., Summerfelt A., McMahon R., Adami H., Francis G., Elliott A., et al. Evoked gamma band synchronization and the liability for schizophrenia. Schizophr Res 2004, 70(2-3):293-302.
20. Hubl D., Koenig T., Strik W.K., Melie Garcia L., Dierks T. Competition for neuronal resources: how hallucinations make themselves heard. Br J Psychiatry 2007, 190:57-62.
21. Hubl D., Hauf M., van Swam C., Muri R., Dierks T., Strik W. Hearing dysphasic voices. Lancet 2007, 370:538.
22. Hubl D., Dougoud-Chauvin V., Zeller M., Federspiel A., Boesch C., Strik W., Dierks T., Koenig T. Structural analysis of Heschl's gyrus in schizophrenia patients with auditory hallucinations. Neuropsychobiology 2010, 61(1):1-9.
23. Jerger J., Chmiel R., Frost J.D., Coker N. Effect of sleep on the auditory steady state evoked potential. Ear Hear 1986, 7(4):240-245.
24. Kalcher J., Pfurtscheller G. Discrimination between phase-locked and non-phase-locked event-related EEG activity. Electroencephalogr Clin Neurophysiol 1995, 94(5):381-384.
25. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 1987, 13(2):261-276.
26. Kindler J., Jann K., Homan P., Hauf M., Walther S., Strik W., Dierks T., Hubl D. Static and dynamic characteristics of cerebral blood flow during the resting state in schizophrenia. Schizophr Bull 2015, 41(1):163-170.
27. Kindler J., Homan P., Jann K., Federspiel A., Flury R., Hauf M., Strik W., Dierks T., Hubl D. Reduced neuronal activity in language-related regions after transcranial magnetic stimulation therapy for auditory verbal hallucinations. Biol Psychiatry 2013, 73(6):518-524.
28. Koenig T., van Swam C., Dierks T., Hubl D. Is gamma band EEG synchronization reduced during auditory driving in schizophrenia patients with auditory verbal hallucinations?. Schizophr Res 2012, 141(2-3):266-270.
29. Kottlow M., Jann K., Dierks T., Koenig T. Increased phase synchronization during continuous face integration measured simultaneously with EEG and fMRI. Clin Neurophysiol 2012, 123(8):1536-1548.
30. Kuriki S., Kobayashi Y., Kobayashi T., Tanaka K., Uchikawa Y. Steady-state MEG responses elicited by a sequence of amplitude-modulated short tones of different carrier frequencies. Hear Res 2013, 296:25-35.
31. Light G.A., Hsu J.L., Hsieh M.H., Meyer-Gomes K., Sprock J., Swerdlow N.R., Braff D.L. Gamma band oscillations reveal neural network cortical coherence dysfunction in schizophrenia patients. Biol Psychiatry 2006, 60(11):1231-1240.
32. Linden R.D., Picton T.W., Hamel G., Campbell K.B. Human auditory steady-state evoked potentials during selective attention. Electroencephalogr Clin Neurophysiol 1987, 66(2):145-159.
33. McFadden K.L., Steinmetz S.E., Carroll A.M., Simon S.T., Wallace A., Rojas D.C. Test-retest reliability of the 40 Hz EEG auditory steady-state response. PLoS One 2014, 9(1):e85748.
34. Mørup M., Hansen L.K., Arnfred S.M. ERPWAVELAB a toolbox for multi-channel analysis of time-frequency transformed event related potentials. J Neurosci Methods 2007, 161(2):361-368.
35. National Institute of Mental Health. CGI: Clinical Global Impressions. In: Guy W., Bonato R.R., editors. Manual for the ECDEU Assessment Battery, 2, Revised Edition. Chevy Chase, Md: National Institute of Mental Health. 1970. 12-1-12-6.
36. Noh K., Shin K.S., Shin D., Hwang J.Y., Kim J.S., Jang J.H., Chung C.K., Kwon J.S., Cho K.H. Impaired coupling of local and global functional feedbacks underlies abnormal synchronization and negative symptoms of schizophrenia. BMC Syst Biol 2013, 7:30.
37. O'Donnell B.F., Vohs J.L., Krishnan G.P., Rass O., Hetrick W.P., Morzorati S.L. The auditory steady-state response (ASSR): a translational biomarker for schizophrenia. Suppl Clin Neurophysiol 2013, 62:101-112.
38. Oulis P.G., Mavreas V.G., Mamounas J.M., Stefanis C.N. Clinical characteristics of auditory hallucinations. Acta Psychiatr Scand 1995, 92(2):97-102.
39. Pantev C., Roberts L.E., Elbert T., Rob B., Wienbruch C. Tonotopic organization of the sources of human auditory steady-state responses. Hear Res 1996, 101(1-2):62-74.
40. Perez V.B., Roach B.J., Woods S.W., Srihari V.H., McGlashan T.H., Ford J.M., Mathalon D.H. Early auditory gamma-band responses in patients at clinical high risk for schizophrenia. Suppl Clin Neurophysiol 2013, 62:147-162.
41. Perrin F., Pernier J., Bertrand O., Echallier J.F. Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 1989, 72(2):184-187.
42. Qin P., Grimm S., Duncan N.W., Holland G., Guo J.S., Fan Y., Weigand A., Baudewig J., Bajbouj M., Northoff G. Self-specific stimuli interact differently than non-self-specific stimuli with eyes-open versus eyes-closed spontaneous activity in auditory cortex. Front Hum Neurosci 2013, 7:437.
43. Rass O., Forsyth J.K., Krishnan G.P., Hetrick W.P., Klaunig M.J., Breier A., et al. Auditory steady state response in the schizophrenia, first-degree relatives, and schizotypal personality disorder. Schizophr Res 2012, 136(1-3):143-149.
44. Roach B.J., Ford J.M., Hoffman R.E., Mathalon D.H. Converging evidence for gamma synchrony deficits in schizophrenia. Suppl Clin Neurophysiol 2013, 62:163-180.
45. Roach B.J., Mathalon D.H. Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. Schizophr Bull 2008, 34(5):907-926.
46. Rojas D.C., Teale P.D., Maharajh K., Kronberg E., Youngpeter K., Wilson L.B., Wallace A., Hepburn S. Transient and steady-state auditory gamma-band responses in first-degree relatives of people with autism spectrum disorder. Mol Autism 2011, 2:11.
47. Ross B., Picton T.W., Herdman A.T., Pantev C. The effect of attention on the auditory steady-state response. Neurol Clin Neurophysiol 2004, 2004:22.
48. Ross B., Herdman A.T., Pantev C. Stimulus induced desynchronization of human auditory 40-Hz steady-state responses. J Neurophysiol 2005, 94(6):4082-4093.
49. Schneider K. Clinical psychopathol 1959, Grune and Stratton, New York.
50. Skosnik P.D., Krishnan G.P., O'Donnell B.F. The effect of selective attention on the gamma-band auditory steady-state response. Neurosci Lett 2007, 420(3):223-228.
51. Smith D.M., Grant B., Fisher D.J., Borracci G., Labelle A., Knott V.J. Auditory verbal hallucinations in schizophrenia correlate with P50 gating. Clin Neurophysiol 2013, 124(7):1329-1335.
52. Smucny J., Olincy A., Eichman L.C., Lyons E., Tregellas J.R. Early sensory processing deficits predict sensitivity to distraction in schizophrenia. Schizophr Res 2013, 147(1):196-200.
53. Smucny J., Wylie K., Rojas D., Stevens K., Olincy A., Kronberg E., Zheng L., Tregellas J. Evidence for gamma and beta sensory gating deficits as translational endophenotypes for schizophrenia. Psychiatry Res 2013, 214(2):169-174.
54. Spencer K.M., Niznikiewicz M.A., Nestor P.G., Shenton M.E., McCarley R.W. Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia. BMC Neurosci 2009, 10:85.
55. Spencer K.M., Salisbury D.F., Shenton M.E., McCarley R.W. Gamma-band auditory steady-state responses are impaired in first episode psychosis. Biol Psychiatry 2008, 64(5):369-375.
56. Tada M., Nagai T., Kirihara K., Koike S., Suga M., Araki T., et al. Differential alterations of auditory gamma oscillatory responses between pre-onset high-risk individuals and first-episode schizophrenia 2014, Cereb Cortex. 10.1093/cercor/bhu278.
57. Tallon-Baudry C., Bertrand O. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 1999, 3(4):151-162.
58. Tan H.R., Gross J., Uhlhaas P.J. MEG-measured auditory steady-state oscillations show high test-retest reliability: a sensor and source-space analysis. NeuroImage 2015, 122:417-426.
59. Teale P., Carlson J., Rojas D., Reite M. Reduced laterality of the source locations for generators of the auditory steady-state field in schizophrenia. Biol Psychiatry 2003, 54(11):1149-1153.
60. Tsuchimoto R., Kanba S., Hirano S., Oribe N., Ueno T., Hirano Y., et al. Reduced high and low frequency gamma synchronization in patients with chronic schizophrenia. Schizophr Res 2011, 133(1-3):99-105.
61. Uhlhaas P.J., Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 2010, 11(2):100-113.
62. Ying J., Zhou D., Lin K., Gao X. Network analysis of functional brain connectivity driven by gamma-band auditory steady-state response in auditory hallucinations. J Med Biol Eng 2015, 35(1):45-51.
63. Yuan B.K., Wang J., Zang Y.F., Liu D.Q. Amplitude differences in high-frequency fMRI signals between eyes open and eyes closed resting states. Front Hum Neurosci 2014, 8:503.
64. Zou Q., Yuan B.K., Gu H., Liu D., Wang D.J., Gao J.H., Yang Y., Zang Y.F. Detecting static and dynamic differences between eyes-closed and eyes-open resting states using ASL and BOLD fMRI. PLoS One 2015, 10(3):e0121757.