Abstract
’Sensing the self’ relies on the ability to distinguish self-generated from external stimuli. It requires functioning mechanisms to establish feelings of agency and ownership. Agency is defined causally, where the subjects action is followed by an effect. Ownership is defined by the features of the effect, independent from the action. In our study, we manipulated these qualities separately. 13 right-handed healthy individuals performed the experiment while 76-channel EEG was recorded. Stimuli consisted of visually presented words, read aloud by the subject. The experiment consisted of six conditions: (a) subjects saw a word, read it aloud, heard it in their own voice; (b) like a, but the word was heard in an unfamiliar voice; (c) subject heard a word in his/her own voice without speaking; (d) like c, but the word was heard in an unfamiliar voice; (e) like a, but subjects heard the word with a delay; (f) subjects read without hearing. ERPs and difference maps were computed for all conditions. Effects were analysed topographically. The N100 (86–172 ms) displayed significant main effects of agency and ownership. The topographies of the two effects shared little common variance, suggesting independent effects. Later effects (174–400 ms) of agency and ownership were topographically similar, suggesting common mechanisms. Replicating earlier studies, significant N100 suppression was observed, with a topography resembling the agency effect. ‘Sensing the self’ appears to recruit from at least two very distinct processes: an agency assessment that represents causality and an ownership assessment that compares stimulus features with memory content.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen P, Amaro E, Fu CH, Williams SC, Brammer MJ, Johns LC, McGuire PK (2007) Neural correlates of the misattribution of speech in schizophrenia. Br J Psychiatry 190:162–169
Baess P, Horvath J, Jacobsen T, Schroger E (2011) Selective suppression of self-initiated sounds in an auditory stream: an ERP study. Psychophysiology 48(9):1276–1283
Behroozmand R, Larson CR (2011) Error-dependent modulation of speech induced auditory suppression for pitch-shifted voice feedback. BMC Neurosci. doi:10.1186/1471-2202-12-54
Blakemore SJ, Wolpert D, Frith C (2000) Why can’t you tickle yourself? NeuroReport 11:R11–R16
Blakemore SJ, Wolpert DM, Frith CD (2002) Abnormalities in the awareness of action. Trends Cogn Sci 6:237–242
Crapse TB, Sommer MA (2008) Corollary discharge across the animal kingdom. Nat Rev Neurosci 9:587–600
Curio G, Neuloh G, Numminen J, Jousmaki V, Hari R (2000) Speaking modifies voice-evoked activity in the human auditory cortex. Hum Brain Mapp 9:183–191
Dierks T, Linden DE, Jandl M, Formisano E, Goebel R, Lanfermann H, Singer W (1999) Activation of Heschl’s gyrus during auditory hallucinations. Neuron 22:615–621
Eichele T, Nordby H, Rimol LM, Hugdahl K (2005) Asymmetry of evoked potential latency to speech sounds predicts the ear advantage in dichotic listening. Brain Res Cogn Brain Res 24:405–412
Feinberg I (1978) Efference copy and corollary discharge: implications for thinking and its disorders. Schizophr Bull 4:636–640
Fiez JA, Petersen SE (1998) Neuroimaging studies of word reading. PNAS USA 95:914–921
Ford JM, Mathalon DH, Heinks T, Kalba S, Faustman WO, Roth WT (2001a) Neurophysiological evidence of corollary discharge dysfunction in schizophrenia. Am J Psychiatry 158:2069–2071
Ford JM, Mathalon DH, Kalba S, Whitfield S, Faustman WO, Roth WT (2001b) Cortical responsiveness during talking and listening in schizophrenia: an event-related brain potential study. Biol Psychiatry 50:540–549
Ford JM, Gray M, Faustman WO, Roach BJ, Mathalon DH (2007) Dissecting corollary discharge dysfunction in schizophrenia. Psychophysiology 44:522–529
Ford JM, Mathalon DH (2012) Anticipating the future: automatic prediction failures in schizophrenia. Int J Psychophysiol 83:232–239
Fu CH, Vythelingum GN, Brammer MJ, Williams SC, Amaro E Jr, Andrew CM, Yaguez L, van Haren NE, Matsumoto K, McGuire PK (2006) An fMRI study of verbal self-monitoring: neural correlates of auditory verbal feedback. Cereb Cortex 16:969–977
Gould L, Cummine J, Borowsky R (2012) The cognitive chronometric architecture of reading aloud: semantic and lexical effects on naming onset and duration. Front Hum Neurosci 6:287
Heinks-Maldonado TH, Mathalon DH, Gray M, Ford JM (2005) Fine-tuning of auditory cortex during speech production. Psychophysiology 42:180–190
Heinks-Maldonado TH, Mathalon DH, Houde JF, Gray M, Faustman WO, Ford JM (2007) Relationship of imprecise corollary discharge in schizophrenia to auditory hallucinations. Arch Gen Psychiatry 64:286–296
Helmholtz Hv (1924) Helmholtz’s treatise on physiological optics. Optical Society of America, New York
Holst Ev (1954) Relations between the central nervous system and the peripheral organs. Br J Anim Behav 2:89–94
Houde JF, Jordan MI (1998) Sensorimotor adaptation in speech production. Science 279:1213–1216
Houde JF, Nagarajan SS, Sekihara K, Merzenich MM (2002) Modulation of the auditory cortex during speech: an MEG study. J Cogn Neurosci 14:1125–1138
Hubl D, Koenig T, Strik WK, Garcia LM, Dierks T (2007) Competition for neuronal resources: how hallucinations make themselves heard. Br J Psychiatry 190:57–62
Jackson JH (1958) Selected writings of John Hughlings. Basic Books, New York
Johns LC, McGuire PK (1999) Verbal self-monitoring and auditory hallucinations in schizophrenia. Lancet 353(9151):469–470
Jung TP, Makeig S, Westerfield M, Townsend J, Courchesne E, Sejnowski TJ (2000) Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects. Clin Neurophysiol 111:1745–1758
Kalckert A, Ehrsson HH (2012) Moving a rubber hand that feels like your own: a dissociation of ownership and agency. Front Hum Neurosci 6:40
Koenig T, Kottlow M, Stein M, Melie-Garcia L (2011) Ragu: a free tool for the analysis of EEG and MEG event-related scalp field data using global randomization statistics. Comput Intell Neurosci 2011:938925
Koenig T, van Swam C, Dierks T, Hubl D (2012) Is gamma band EEG synchronization reduced during auditory driving in schizophrenia patients with auditory verbal hallucinations? Schizophr Res 141:266–270
Kottlow M, Jann K, Dierks T, Koenig T (2012) Increased phase synchronization during continuous face integration measured simultaneously with EEG and fMRI. Clin Neurophysiol 123:1536–1548
Leube DT, Knoblich G, Erb M, Grodd W, Bartels M, Kircher TT (2003) The neural correlates of perceiving one’s own movements. Neuroimage 20:2084–2090
Macphee GJ, Crowther JA, McAlpine CH (1988) A simple screening test for hearing impairment in elderly patients. Age Ageing 17:347–351
Maidhof C, Vavatzanidis N, Prinz W, Rieger M, Koelsch S (2010) Processing expectancy violations during music performance and perception: an ERP study. J Cogn Neurosci 22:2401–2413
McCarthy-Jones S, Trauer T, Mackinnon A, Sims E, Thomas N, Copolov DL (2012) A new phenomenological survey of auditory hallucinations: evidence for subtypes and implications for theory and practice. Schizophr Bull. doi:10.1093/schbul/sbs156
Michel CM, Koenig T, Brandeis D (2009) Electrical neuroimaging in the time domain. In: Michel CM, Koenig T, Brandeis D, Gianotti LRR, Wackermann J (eds) Electrical neuroimaging. Cambridge University Press, New York, pp 111–143
Nahab FB, Kundu P, Gallea C, Kakareka J, Pursley R, Pohida T, Miletta N, Friedman J, Hallett M (2011) The neural processes underlying self-agency. Cereb Cortex 21:48–55
Pantev C, Hoke M, Lehnertz K, Lutkenhoner B, Anogianakis G, Wittkowski W (1988) Tonotopic organization of the human auditory cortex revealed by transient auditory evoked magnetic fields. Electroencephalogr Clin Neurophysiol 69:160–170
Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12
Raij TT, Valkonen-Korhonen M, Holi M, Therman S, Lehtonen J, Hari R (2009) Reality of auditory verbal hallucinations. Brain 132:2994–3001
Sperry RW (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43(6):482–489
Strik WK, Fallgatter AJ, Brandeis D, Pascual-Marqui RD (1998) Three-dimensional tomography of event-related potentials during response inhibition: evidence for phasic frontal lobe activation. Electroencephalogr Clin Neurophysiol 108:406–413
Synofzik M, Vosgerau G, Voss M (2013) The experience of agency: an interplay between prediction and postdiction. Front Psychol 4:127
van Veen V, Carter CS (2002) The anterior cingulate as a conflict monitor: fMRI and ERP studies. Physiol Behav 77:477–482
Wang L, Metzak PD, Woodward TS (2011) Aberrant connectivity during self-other source monitoring in schizophrenia. Schizophr Res 125:136–142
Wirth M, Horn H, Koenig T, Razafimandimby A, Stein M, Mueller T, Federspiel A, Meier B, Dierks T, Strik W (2008) The early context effect reflects activity in the temporo-prefrontal semantic system: evidence from electrical neuroimaging of abstract and concrete word reading. Neuroimage 42:423–436
Wirth M, Jann K, Dierks T, Federspiel A, Wiest R, Horn H (2011) Semantic memory involvement in the default mode network: a functional neuroimaging study using independent component analysis. Neuroimage 54:3057–3066
Wurtz RH (2008) Neuronal mechanisms of visual stability. Vision Res 48:2070–2089
Acknowledgments
We are grateful to Miranka Wirth for providing the word stimuli. Further, we thank Nicolas Moor for testing out different delays.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hubl, D., Schneider, R.C., Kottlow, M. et al. Agency and Ownership are Independent Components of ‘Sensing the Self’ in the Auditory-Verbal Domain. Brain Topogr 27, 672–682 (2014). https://doi.org/10.1007/s10548-014-0351-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-014-0351-0