Skip to main content
Log in

Generators and Connectivity of the Early Auditory Evoked Gamma Band Response

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

High frequency oscillations in the gamma range are known to be involved in early stages of auditory information processing in terms of synchronization of brain regions, e.g., in cognitive functions. It has been shown using EEG source localisation, as well as simultaneously recorded EEG-fMRI, that the auditory evoked gamma-band response (aeGBR) is modulated by attention. In addition to auditory cortex activity a dorsal anterior cingulate cortex (dACC) generator could be involved. In the present study we investigated aeGBR magnetic fields using magnetoencephalography (MEG). We aimed to localize the aeGBR sources and its connectivity features in relation to mental effort. We investigated the aeGBR magnetic fields in 13 healthy participants using a 275-channel CTF-MEG system. The experimental paradigms were two auditory choice reaction tasks with different difficulties and demands for mental effort. We performed source localization with eLORETA and calculated the aeGBR lagged phase synchronization between bilateral auditory cortices and frontal midline structures. The eLORETA analysis revealed sources of the aeGBR within bilateral auditory cortices and in frontal midline structures of the brain including the dACC. Compared to the control condition the dACC source activity was found to be significantly stronger during the performance of the cognitively demanding task. Moreover, this task involved a significantly stronger functional connectivity between auditory cortices and dACC. In accordance with previous EEG and EEG-fMRI investigations, our study confirms an aeGBR generator in the dACC by means of MEG and suggests its involvement in the effortful processing of auditory stimuli.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aboitiz F, Lopez J, Montiel J (2003) Long distance communication in the human brain: timing constraints for inter-hemispheric synchrony and the origin of brain lateralization. Biol Res 36(1):89–99

    Article  PubMed  Google Scholar 

  • Ahveninen J, Kahkonen S, Tiitinen H, Pekkonen E, Huttunen J, Kaakkola S, Ilmoniemi RJ, Jaaskelainen IP (2000) Suppression of transient 40-Hz auditory response by haloperidol suggests modulation of human selective attention by dopamine D2 receptors. Neurosci Lett 292(1):29–32

    Article  CAS  PubMed  Google Scholar 

  • Ahveninen J, Huang S, Belliveau JW, Chang WT, Hamalainen M (2013) Dynamic oscillatory processes governing cued orienting and allocation of auditory attention. J Cogn Neurosci 25(11):1926–1943

    Article  PubMed Central  PubMed  Google Scholar 

  • Barth DS, MacDonald KD (1996) Thalamic modulation of high-frequency oscillating potentials in auditory cortex. Nature 383(6595):78–81

    Article  CAS  PubMed  Google Scholar 

  • Basar E (2013) A review of gamma oscillations in healthy subjects and in cognitive impairment. Int J Psychophysiol 90(2):99–117

    Article  PubMed  Google Scholar 

  • Bastiaansen MCM, Knosche TR (2000) Tangential derivative mapping of axial MEG applied to event-related desynchronization research. Clin Neurophysiol 111(7):1300–1305

    Article  CAS  PubMed  Google Scholar 

  • Bénar CG, Bagshaw AP, Lemieux L (2010) Experimental design and data analysis strategies. In: Mulert C, Lemieux L (eds) EEG-fMRI—physiological basis, technique, and applications. Springer, Berlin, pp 221–257

    Google Scholar 

  • Bhattacharya J, Petsche H, Pereda E (2001) Long-range synchrony in the gamma band: role in music perception. J Neurosci 21(16):6329–6337

    CAS  PubMed  Google Scholar 

  • Botvinick M, Nystrom LE, Fissell K, Carter CS, Cohen JD (1999) Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402(6758):179–181

    Article  CAS  PubMed  Google Scholar 

  • Brosch M, Budinger E, Scheich H (2002) Stimulus-related gamma oscillations in primate auditory cortex. J Neurophysiol 87(6):2715–2725

    PubMed  Google Scholar 

  • Bush G, Whalen PJ, Rosen BR, Jenike MA, McInerney SC, Rauch SL (1998) The counting Stroop: an interference task specialized for functional neuroimaging–validation study with functional MRI. Hum Brain Mapp 6(4):270–282

    Article  CAS  PubMed  Google Scholar 

  • Bush G, Vogt BA, Holmes J, Dale AM, Greve D, Jenike MA, Rosen BR (2002) Dorsal anterior cingulate cortex: a role in reward-based decision making. Proc Natl Acad Sci USA 99(1):523–528

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926–1929

    Article  CAS  PubMed  Google Scholar 

  • Buzsaki G, Wang XJ (2012) Mechanisms of gamma oscillations. Annu Rev Neurosci 35:203–225

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends in Cogn Sci 14(11):506–515

    Article  Google Scholar 

  • Carl C, Acik A, Konig P, Engel AK, Hipp JF (2012) The saccadic spike artifact in MEG. Neuroimage 59(2):1657–1667

    Article  PubMed  Google Scholar 

  • Debener S, Herrmann CS, Kranczioch C, Gembris D, Engel AK (2003) Top-down attentional processing enhances auditory evoked gamma band activity. NeuroReport 14(5):683–686

    Article  PubMed  Google Scholar 

  • Edwards E, Soltani M, Deouell LY, Berger MS, Knight RT (2005) High gamma activity in response to deviant auditory stimuli recorded directly from human cortex. J Neurophysiol 94(6):4269–4280

    Article  PubMed  Google Scholar 

  • Fell J, Fernandez G, Klaver P, Elger CE, Fries P (2003) Is synchronized neuronal gamma activity relevant for selective attention? Brain Res Brain Res Rev 42(3):265–272

    Article  PubMed  Google Scholar 

  • Fiehler K, Ullsperger M, von Cramon DY (2004) Neural correlates of error detection and error correction: is there a common neuroanatomical substrate? Eur J Neurosci 19(11):3081–3087

    Article  PubMed  Google Scholar 

  • Fontolan L, Morillon B, Liegeois-Chauvel C, Giraud AL (2014) The contribution of frequency-specific activity to hierarchical information processing in the human auditory cortex. Nat Commun 5:4694

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RS (1994) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2(4):189–210

    Article  Google Scholar 

  • Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, Lebeau FE, Bannerman DM, Rozov A, Whittington MA, Traub RD, Rawlins JN et al (2007) Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53(4):591–604

    Article  CAS  PubMed  Google Scholar 

  • Gurtubay IG, Alegre M, Labarga A, Malanda A, Artieda J (2004) Gamma band responses to target and non-target auditory stimuli in humans. Neurosci Lett 367(1):6–9

    Article  CAS  PubMed  Google Scholar 

  • Herrmann CS, Munk MH, Engel AK (2004) Cognitive functions of gamma-band activity: memory match and utilization. Trends Cogn Sci 8(8):347–355

    Article  PubMed  Google Scholar 

  • Herrmann CS, Frund I, Lenz D (2010) Human gamma-band activity: a review on cognitive and behavioral correlates and network models. Neurosci Biobehav Rev 34(7):981–992

    Article  PubMed  Google Scholar 

  • Hipp JF, Hawellek DJ, Corbetta M, Siegel M, Engel AK (2012) Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat Neurosci 15(6):884–890

    Article  CAS  PubMed  Google Scholar 

  • Hirano S, Hirano Y, Maekawa T, Obayashi C, Oribe N, Kuroki T, Kanba S, Onitsuka T (2008) Abnormal neural oscillatory activity to speech sounds in schizophrenia: a magnetoencephalography study. J Neurosci 28(19):4897–4903

    Article  CAS  PubMed  Google Scholar 

  • Hirata M, Koreeda S, Sakihara K, Kato A, Yoshimine T, Yorifuji S (2007) Effects of the emotional connotations in words on the frontal areas—a spatially filtered MEG study. Neuroimage 35(1):420–429

    Article  PubMed  Google Scholar 

  • Holroyd CB, Yeung N (2012) Motivation of extended behaviors by anterior cingulate cortex. Trends Cogn Sci 16(2):122–128

    Article  PubMed  Google Scholar 

  • Jensen O, Colgin LL (2007) Cross-frequency coupling between neuronal oscillations. Trends Cogn Sci 11(7):267–269

    Article  PubMed  Google Scholar 

  • Johannesen JK, Bodkins M, O’Donnell BF, Shekhar A, Hetrick WP (2008) Perceptual anomalies in schizophrenia co-occur with selective impairments in the gamma frequency component of midlatency auditory ERPs. J Abnorm Psychol 117(1):106–118

    Article  PubMed  Google Scholar 

  • Leicht G, Kirsch V, Giegling I, Karch S, Hantschk I, Moller HJ, Pogarell O, Hegerl U, Rujescu D, Mulert C (2010) Reduced early auditory evoked gamma-band response in patients with schizophrenia. Biol Psychiatry 67(3):224–231

    Article  PubMed  Google Scholar 

  • Leicht G, Karch S, Karamatskos E, Giegling I, Moller HJ, Hegerl U, Pogarell O, Rujescu D, Mulert C (2011) Alterations of the early auditory evoked gamma-band response in first-degree relatives of patients with schizophrenia: hints to a new intermediate phenotype. J Psychiatr Res 45(5):699–705

    Article  PubMed  Google Scholar 

  • Lisman JE, Jensen O (2013) The theta-gamma neural code. Neuron 77(6):1002–1016

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Makeig S, Bell AJ, Jung TP, Sejnowski TJ (1996) Independent component analysis of electroencephalographic data. Adv Neural Inf Process Syst 8:145–151

    Google Scholar 

  • Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233–1239

    Article  PubMed  Google Scholar 

  • Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, Paus T, Simpson G, Pike B et al (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356(1412):1293–1322

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mega MS, Cummings JL (1996) The cingulate and cingulate syndromes. In: Trimble M, Cummings LJ (eds) Contemporary behavioral neurology, 1st edn. Butterworth-Heinemann, Oxford, pp 189–214

    Google Scholar 

  • Mulert C, Gallinat J, Pascual-Marqui R, Dorn H, Frick K, Schlattmann P, Mientus S, Herrmann WM, Winterer G (2001) Reduced event-related current density in the anterior cingulate cortex in schizophrenia. Neuroimage 13(4):589–600

    Article  CAS  PubMed  Google Scholar 

  • Mulert C, Gallinat J, Dorn H, Herrmann WM, Winterer G (2003) The relationship between reaction time, error rate and anterior cingulate cortex activity. Int J Psychophysiol 47(2):175–183

    Article  PubMed  Google Scholar 

  • Mulert C, Jager L, Propp S, Karch S, Stormann S, Pogarell O, Moller HJ, Juckel G, Hegerl U (2005a) Sound level dependence of the primary auditory cortex: simultaneous measurement with 61-channel EEG and fMRI. Neuroimage 28(1):49–58

    Article  PubMed  Google Scholar 

  • Mulert C, Menzinger E, Leicht G, Pogarell O, Hegerl U (2005b) Evidence for a close relationship between conscious effort and anterior cingulate cortex activity. Int J Psychophysiol 56(1):65–80

    Article  PubMed  Google Scholar 

  • Mulert C, Leicht G, Pogarell O, Mergl R, Karch S, Juckel G, Moller HJ, Hegerl U (2007) Auditory cortex and anterior cingulate cortex sources of the early evoked gamma-band response: relationship to task difficulty and mental effort. Neuropsychologia 45(10):2294–2306

    Article  PubMed  Google Scholar 

  • Mulert C, Seifert C, Leicht G, Kirsch V, Ertl M, Karch S, Moosmann M, Lutz J, Moller HJ, Hegerl U et al (2008) Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making. Neuroimage 42(1):158–168

    Article  PubMed  Google Scholar 

  • Mulert C, Leicht G, Hepp P, Kirsch V, Karch S, Pogarell O, Reiser M, Hegerl U, Jager L, Moller HJ et al (2010) Single-trial coupling of the gamma-band response and the corresponding BOLD signal. Neuroimage 49(3):2238–2247

    Article  CAS  PubMed  Google Scholar 

  • Mulert C, Kirsch V, Pascual-Marqui R, McCarley RW, Spencer KM (2011) Long-range synchrony of gamma oscillations and auditory hallucination symptoms in schizophrenia. Int J Psychophysiol 79(1):55–63

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nolte G (2003) The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. Phys Med Biol 48(22):3637–3652

    Article  PubMed  Google Scholar 

  • Oostenveld R, Fries P, Maris E, Schoffelen JM (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869

    PubMed Central  PubMed  Google Scholar 

  • Palva S, Palva JM, Shtyrov Y, Kujala T, Ilmoniemi RJ, Kaila K, Naatanen R (2002) Distinct gamma-band evoked responses to speech and non-speech sounds in humans. J Neurosci 22(4):RC211

    PubMed  Google Scholar 

  • Pandya DN, Van Hoesen GW, Mesulam MM (1981) Efferent connections of the cingulate gyrus in the rhesus monkey. Exp Brain Res 42(3–4):319–330

    Article  CAS  PubMed  Google Scholar 

  • Pantev C, Makeig S, Hoke M, Galambos R, Hampson S, Gallen C (1991) Human auditory evoked gamma-band magnetic fields. Proc Natl Acad Sci USA 88(20):8996–9000

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pascual-Marqui RD (2007a) Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization. arXiv:0710.3341 [math-ph]

  • Pascual-Marqui RD (2007b) Instantaneous and lagged measurements of linear and nonlinear dependence between groups of multivariate time series: frequency decomposition. arXiv:0711.1455[stat.ME]

  • Perez VB, Roach BJ, Woods SW, Srihari VH, McGlashan TH, Ford JM, Mathalon DH (2013) Early auditory gamma-band responses in patients at clinical high risk for schizophrenia. Suppl Clin Neurophysiol 62:147–162

    Article  PubMed Central  PubMed  Google Scholar 

  • Perianez JA, Maestu F, Barcelo F, Fernandez A, Amo C, Ortiz Alonso T (2004) Spatiotemporal brain dynamics during preparatory set shifting: MEG evidence. Neuroimage 21(2):687–695

    Article  PubMed  Google Scholar 

  • Ribary U, Ioannides AA, Singh KD, Hasson R, Bolton JP, Lado F, Mogilner A, Llinas R (1991) Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc Natl Acad Sci USA 88(24):11037–11041

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roach BJ, Mathalon DH (2008) Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. Schizophr Bull 34(5):907–926

    Article  PubMed Central  PubMed  Google Scholar 

  • Ross B, Picton TW, Pantev C (2002) Temporal integration in the human auditory cortex as represented by the development of the steady-state magnetic field. Hear Res 165(1–2):68–84

    Article  PubMed  Google Scholar 

  • Ross B, Herdman AT, Pantev C (2005) Right hemispheric laterality of human 40 Hz auditory steady-state responses. Cereb Cortex 15(12):2029–2039

    Article  CAS  PubMed  Google Scholar 

  • Roux F, Wibral M, Singer W, Aru J, Uhlhaas PJ (2013) The phase of thalamic alpha activity modulates cortical gamma-band activity: evidence from resting-state MEG recordings. J Neurosci 33(45):17827–17835

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schadow J, Lenz D, Thaerig S, Busch NA, Frund I, Herrmann CS (2007) Stimulus intensity affects early sensory processing: sound intensity modulates auditory evoked gamma-band activity in human EEG. Int J Psychophysiol 65(2):152–161

    Article  PubMed  Google Scholar 

  • Schadow J, Lenz D, Dettler N, Frund I, Herrmann CS (2009) Early gamma-band responses reflect anticipatory top-down modulation in the auditory cortex. Neuroimage 47(2):651–658

    Article  PubMed  Google Scholar 

  • Sedley W, Teki S, Kumar S, Barnes GR, Bamiou DE, Griffiths TD (2012) Single-subject oscillatory gamma responses in tinnitus. Brain 135(Pt 10):3089–3100

    Article  PubMed Central  PubMed  Google Scholar 

  • Senkowski D, Talsma D, Grigutsch M, Herrmann CS, Woldorff MG (2007) Good times for multisensory integration: effects of the precision of temporal synchrony as revealed by gamma-band oscillations. Neuropsychologia 45(3):561–571

    Article  PubMed  Google Scholar 

  • Shenhav A, Botvinick MM, Cohen JD (2013) The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron 79(2):217–240

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sheth SA, Mian MK, Patel SR, Asaad WF, Williams ZM, Dougherty DD, Bush G, Eskandar EN (2012) Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation. Nature 488(7410):218–221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24(1):49–65 111–25

    Article  CAS  PubMed  Google Scholar 

  • Srinivasan L, Asaad WF, Ginat DT, Gale JT, Dougherty DD, Williams ZM, Sejnowski TJ, Eskandar EN (2013) Action initiation in the human dorsal anterior cingulate cortex. PLoS ONE 8(2):e55247

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steinmann S, Leicht G, Ertl M, Andreou C, Polomac N, Westerhausen R, Friederici AD, Mulert C (2014) Conscious auditory perception related to long-range synchrony of gamma oscillations. Neuroimage 100:435–443

    Article  PubMed  Google Scholar 

  • Steinschneider M, Fishman YI, Arezzo JC (2008) Spectrotemporal analysis of evoked and induced electroencephalographic responses in primary auditory cortex (A1) of the awake monkey. Cereb Cortex 18(3):610–625

    Article  PubMed  Google Scholar 

  • Tiitinen H, Sinkkonen J, Reinikainen K, Alho K, Lavikainen J, Naatanen R (1993) Selective attention enhances the auditory 40-Hz transient response in humans. Nature 364(6432):59–60

    Article  CAS  PubMed  Google Scholar 

  • Tiitinen H, May P, Naatanen R (1997) The transient 40-Hz response, mismatch negativity, and attentional processes in humans. Prog Neuropsychopharmacol Biol Psychiatry 21(5):751–771

    Article  CAS  PubMed  Google Scholar 

  • Turken AU, Swick D (1999) Response selection in the human anterior cingulate cortex. Nat Neurosci 2(10):920–924

    Article  CAS  PubMed  Google Scholar 

  • Uhlhaas PJ, Singer W (2010) Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11(2):100–113

    Article  CAS  PubMed  Google Scholar 

  • Uhlhaas PJ, Singer W (2013) High-frequency oscillations and the neurobiology of schizophrenia. Dialogues Clin Neurosci 15(3):301–313

    PubMed Central  PubMed  Google Scholar 

  • van Wijk BC, Fitzgerald TH (2014) Thalamo-cortical cross-frequency coupling detected with MEG. Front Hum Neurosci 8:187

    PubMed Central  PubMed  Google Scholar 

  • Vogt BA (2009) Regions and subregions of the cingulate cortex. In: Vogt BA (ed) Cingulate neurobiology and disease. Oxford University Press Inc., New York, pp 3–30

    Google Scholar 

  • Vogt BA, Pandya DN (1987) Cingulate cortex of the rhesus monkey: II. Cortical afferents. J Comp Neurol 262(2):271–289

    Article  CAS  PubMed  Google Scholar 

  • Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373(6515):612–615

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christoph Mulert.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Polomac, N., Leicht, G., Nolte, G. et al. Generators and Connectivity of the Early Auditory Evoked Gamma Band Response. Brain Topogr 28, 865–878 (2015). https://doi.org/10.1007/s10548-015-0434-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-015-0434-6

Keywords

Navigation