Abstract
Knowledge about the effects of our actions is an underlying feature of voluntary behavior. Given the importance of identifying the outcomes of our actions, it has been proposed that the sensory outcomes of self-made actions are inherently different from those of externally caused outcomes. Thus, the outcomes of self-made actions are likely to be more motivationally significant for an agent. We used event-related potentials to investigate the relationship between the perceived motivational significance of an outcome and the attribution of agency in the presence of others. In our experiment, we assessed agency attribution in the presence of another agent by varying the degree of contiguity between participants’ self-made actions and the sensory outcome. Specifically, we assessed the feedback correct-related positivity (fCRP) and the novelty P3 measures of an outcome’s motivational significance and unexpectedness, respectively. Results revealed that both the fCRP and participants’ agency attributions were significantly influenced by action–outcome contiguity. However, when action–outcome contiguity was ambiguous, novelty P3 amplitude was a reliable indicator of agency attribution. Prior agency attributions were also found to influence attribution in trials with ambiguous and low action–outcome contiguity. Participants’ use of multiple cues to determine agency is consistent with the cue integration theory of agency. In addition to these novel findings, this study supports growing evidence suggesting that reinforcement processes play a significant role in the sense of agency.
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References
Abi-Dargham A, Gil R, Krystal J, Baldwin RM, Seibyl JP, Bowers M, van Dyck CH, Charney DS, Innis RB, Laruelle M (1998) Increased striatal dopamine transmission in schizophrenia: confirmation in a second cohort. Am J Psychiatr 155(6):761–767
Baess P, Jacobsen T, Schroeger E (2008) Suppression of the auditory N1 event-related potential component with unpredictable self-initiated tones: evidence for internal forward models with dynamic stimulation. Int J Psychophysiol 70(2):137–143. doi:10.1016/j.ijpsycho.2008.06.005
Bednark JG, Reynolds JNJ, Stafford T, Redgrave P, Franz EA (2013) Creating a movement heuristic for voluntary action: electrophysiological correlates of movement-outcome learning. Cortex 49(3):771–780. doi:10.1016/j.cortex.2011.12.005
Blakemore SJ, Wolpert D, Frith C (2000) Why can’t you tickle yourself? NeuroReport 11(11):R11
Desantis A, Roussel C, Waszak F (2011) On the influence of causal beliefs on the feeling of agency. Conscious Cogn 20(4):1211–1220. doi:10.1016/j.concog.2011.02.012
Desantis A, Weiss C, Schütz-Bosbach S, Waszak F (2012) Believing and perceiving: authorship belief modulates sensory attenuation. PLoS One 7(5):e37959. doi:10.1371/journal.pone.0037959
Donchin E, Coles MGH (1988) Is the P300 component a manifestation of context updating. Behav Brain Sci 11(3):357–374
Eitam B, Kennedy P, Tory Higgins E (2013) Motivation from control. Exp Brain Res 229(3):475–484. doi:10.1007/s00221-012-3370-7
Elsner B, Hommel B (2001) Effect anticipation and action control. J Exp Psychol Hum Percept Perform 27(1):229–240
Elsner B, Hommel B (2004) Contiguity and contingency in action–effect learning. Psychol Res Psychol Forsch 68(2–3):138–154. doi:10.1007/s00426-003-0151-8
Elsner B, Hommel B, Mentschel C, Drzezga A, Prinz W, Conrad B, Siebner H (2002) Linking actions and their perceivable consequences in the human brain. Neuroimage 17(1):364–372. doi:10.1006/nimg.2002.1162
Foti D, Weinberg A, Dien J, Hajcak G (2011) Event related potential activity in the basal ganglia differentiates rewards from nonrewards: temporospatial principal components analysis and source localization of the feedback negativity. Hum Brain Mapp 32(12):2207–2216. doi:10.1002/hbm.21182
Frank MJ, Seeberger LC, O’Reilly RC (2004) By carrot or by stick: cognitive reinforcement learning in Parkinsonism. Science 306(5703):1940–1943. doi:10.1126/science.1102941
Friedman D, Cycowicz YM, Gaeta H (2001) The novelty P3: an event-related brain potential (ERP) sign of the brain’s evaluation of novelty. Neurosci Biobehav R 25(4):355–373
Gehring WJ, Willoughby AR (2002) The medial frontal cortex and the rapid processing of monetary gains and losses. Science 295(5563):2279–2282
Gentsch A, Schuetz-Bosbach S (2011) I did it: unconscious expectation of sensory consequences modulates the experience of self-agency and its functional signature. J Cogn Neurosci 23(12):3817–3828
Haggard P, Tsakiris M (2009) The experience of agency: feelings, judgments, and responsibility. Curr Dir Psychol 18(4):242–246
Hajcak G, Moser JS, Holroyd CB, Simons RF (2006) The feedback-related negativity reflects the binary evaluation of good versus bad outcomes. Biol Psychol 71(2):148–154. doi:10.1016/j.biopsycho.2005.04.001
Holroyd CB, Coles MGH (2002) The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 109(4):679–709. doi:10.1037//0033-295x.109.4.679
Holroyd CB, Coles MGH (2008) Dorsal anterior cingulate cortex integrates reinforcement history to guide voluntary behavior. Cortex 44(5):548–559
Holroyd CB, Hajcak G, Larsen JT (2006) The good, the bad and the neutral: electrophysiological responses to feedback stimuli. Brain Res 1105:93–101. doi:10.1016/j.brainres.2005.12.015
Holroyd CB, Pakzad-Vaezi KL, Krigolson OE (2008) The feedback correct-related positivity: sensitivity of the event-related brain potential to unexpected positive feedback. Psychophysiology 45(5):688–697. doi:10.1111/j.1469-8986.2008.00668.x
Holroyd CB, Krigolson OE, Lee S (2011) Reward positivity elicited by predictive cues. NeuroReport 22(5):249
Howell DC (2013) Statistical methods for psychology, 8th edn. Wadsworth Cengage Learning, Belmont, CA
Hughes G, Waszak F (2011) ERP correlates of action effect prediction and visual sensory attenuation in voluntary action. Neuroimage 56(3):1632–1640
Hughes G, Desantis A, Waszak F (2013) Attenuation of auditory N1 results from identity-specific action–effect prediction. Eur J Neurosci 37(7):1152–1158. doi:10.1111/ejn.12120
Kenemans J, Kok A, Smulders F (1993) Event-related potentials to conjunctions of spatial frequency and orientation as a function of stimulus parameters and response requirements. Electroencephalogr Clin Neurophysiol/Evoked Potentials Sect 88(1):51–63
Krigolson OE, Holroyd CB, Van Gyn G, Heath M (2008) Electroencephalographic correlates of target and outcome errors. Exp Brain Res 190(4):401–411. doi:10.1007/s00221-008-1482-x
Kuhn S, Nenchev I, Haggard P, Brass M, Gallinat J, Voss M (2011) Whodunnit? Electrophysiological correlates of agency judgements. PLoS One 6(12). doi:10.1371/journal.pone.0028657
Li P, Jia S, Feng T, Liu Q, Suo T, Li H (2010) The influence of the diffusion of responsibility effect on outcome evaluations: electrophysiological evidence from an ERP study. Neuroimage 52(4):1727–1733. doi:10.1016/j.neuroimage.2010.04.275
Li P, Han C, Lei Y, Holroyd CB, Li H (2011) Responsibility modulates neural mechanisms of outcome processing: an ERP study. Psychophysiology 48(8):1129–1133. doi:10.1111/j.1469-8986.2011.01182.x
Luck SJ (2005) An introduction to the event-related potential technique. MIT Press, Cambridge, MA
Makeig S, Westerfield M, Jung TP, Covington J, Townsend J, Sejnowski TJ, Courchesne E (1999) Functionally independent components of the late positive event-related potential during visual spatial attention. J Neurosci 19(7):2665
Moore JW, Fletcher PC (2012) Sense of agency in health and disease: a review of cue integration approaches. Conscious Cogn 21(1):59–68. doi:10.1016/j.concog.2011.08.010
Moore JW, Wegner DM, Haggard P (2009) Modulating the sense of agency with external cues. Conscious Cogn 18(4):1056–1064. doi:10.1016/j.concog.2009.05.004
Moore JW, Schneider SA, Schwingenschuh P, Moretto G, Bhatia KP, Haggard P (2010) Dopaminergic medication boosts action–effect binding in Parkinson’s disease. Neuropsychologia 48(4):1125–1132. doi:10.1016/j.neuropsychologia.2009.12.014
Muhle-Karbe PS, Krebs RM (2012) On the influence of reward on action–effect binding. Front Psychol 3. doi:10.3389/fpsyg.2012.00450
Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2(6):417–424
Peterson DA, Lotz DT, Halgren E, Sejnowski TJ, Poizner H (2010) Choice modulates the neural dynamics of prediction error processing during rewarded learning. Neuroimage 54(2):1385–1394. doi:10.1016/j.neuroimage.2010.09.051
Potts GF, Tucker DM (2001) Frontal evaluation and posterior representation in target detection. Cognit Brain Res 11(1):147–156
Potts GF, Liotti M, Tucker DM, Posner MI (1996) Frontal and inferior temporal cortical activity in visual target detection: evidence from high spatially sampled event-related potentials. Brain Topogr 9(1):3–14
Redgrave P, Gurney K, Reynolds J (2008) What is reinforced by phasic dopamine signals? Brain Res Rev 58(2):322–339. doi:10.1016/J.Brainresrev.10.007
Redgrave P, Vautrelle N, Reynolds JNJ (2011) Functional properties of the basal ganglia’s re-entrant loop architecture: selection and reinforcement. Neuroscience 198:138–151. doi:10.1016/j.neuroscience.2011.07.060
Rilling JK, Gutman DA, Zeh TR, Pagnoni G, Berns GS, Kilts CD (2002) A neural basis for social cooperation. Neuron 35(2):395–405
Rushworth MFS, Behrens TEJ, Rudebeck PH, Walton ME (2007) Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour. Trends Cogn Sci 11(4):168–176. doi:10.1016/j.tics.2007.01.004
Sato A (2009) Both motor prediction and conceptual congruency between preview and action–effect contribute to explicit judgment of agency. Cognition 110(1):74–83. doi:10.1016/j.cognition.2008.10.011
Synofzik M, Vosgerau G, Newen A (2008a) Beyond the comparator model: a multifactorial two-step account of agency. Conscious Cogn 17(1):219–239
Synofzik M, Vosgerau G, Newen A (2008b) I move, therefore I am: a new theoretical framework to investigate agency and ownership. Conscious Cogn 17(2):411–424. doi:10.1016/j.concog.2008.03.008
Synofzik M, Vosgerau G, Voss M (2013) The experience of agency: an interplay between prediction and postdiction. Front Psychol 4. doi:10.3389/fpsyg.2013.00127
Takahata K, Takahashi H, Maeda T, Umeda S, Suhara T, Mimura M, Kato M (2012) It’s not my fault: postdictive modulation of intentional binding by monetary gains and losses. PLoS One 7(12):e53421. doi:10.1371/journal.pone.0053421
Tomlin D, Kayali MA, King-Casas B, Anen C, Camerer CF, Quartz SR, Montague PR (2006) Agent-specific responses in the cingulate cortex during economic exchanges. Science 312(5776):1047–1050
Walton ME, Devlin JT, Rushworth MFS (2004) Interactions between decision making and performance monitoring within prefrontal cortex. Nat Neurosci 7(11):1259–1265. doi:10.1038/nn1339
Wegner DM, Sparrow B (2004) Authorship processing. In: Gazzaniga MS (ed) The new cognitive neurosciences, 3rd edn. MIT Press, Cambridge, MA
Wegner DM, Sparrow B, Winerman L (2004) Vicarious agency: experiencing control over the movements of others. J Pers Soc Psychol 86(6):838
Acknowledgments
The authors would like to acknowledge the contributions of Rebecca Scott, Nigel Barett, and Jeremy Anderson for their assistance in setting up EEG equipment and the use of the Physical Education laboratory at the University of Otago. We also thank Simmy Poonian and Michel Bednark Ohmer for editorial comments. J.G.B. was supported by a University of Otago PhD scholarship, and E.A.F was a recipient of research funding from a University of Otago Research Grant and a Marsden grant from the Royal Society of New Zealand, during the preparation of the manuscript.
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Bednark, J.G., Franz, E.A. Agency attribution: event-related potentials and outcome monitoring. Exp Brain Res 232, 1117–1126 (2014). https://doi.org/10.1007/s00221-014-3821-4
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DOI: https://doi.org/10.1007/s00221-014-3821-4