Modulating human sense of agency with non-invasive brain stimulation

Human voluntary actions are accompanied by a distinctive subjective experience termed "sense of agency". We performed three experiments using transcranial direct current stimulation (tDCS) to modulate brain circuits involved in control of action, while measuring stimulation-induced changes in one implicit measure of sense of agency, namely the perceived temporal relationship between a voluntary action and tone triggered by the action. Participants perceived such tones as shifted towards the action that caused them, relative to baseline conditions with tones but no actions. Actions that caused tones were perceived as shifted towards the tone, relative to baseline actions without tones. This 'intentional binding' was diminished by anodal stimulation of the left parietal cortex [targeting the angular gyrus (AG)], and, to a lesser extent, by stimulation targeting the left dorsolateral prefrontal cortex (DLPFC), (Experiment 1). Cathodal AG stimulation had no effect (Experiment 2). Experiment 3 replicated the effect of left anodal AG stimulation for actions made with either the left or the right hand, and showed no effect of right anodal AG stimulation. The angular gyrus has been identified as a key area for explicit agency judgements in previous neuroimaging and lesion studies. Our study provides new causal evidence that the left angular gyrus plays a key role in the perceptual experience of agency.

[1]  Ulrich Meier,et al.  A note on the power of Fisher's least significant difference procedure , 2006, Pharmaceutical statistics.

[2]  C. Frith,et al.  Experiencing Oneself vs Another Person as Being the Cause of an Action: The Neural Correlates of the Experience of Agency , 2002, NeuroImage.

[3]  R. Klatzky,et al.  Cognitive representations of hand posture in ideomotor apraxia , 2003, Neuropsychologia.

[4]  W. Prinz,et al.  An online neural substrate for sense of agency. , 2013, Cerebral cortex.

[5]  D. Levy,et al.  Oppositional transcranial direct current stimulation (tDCS) of parietal substrates of attention during encoding modulates episodic memory , 2012, Brain Research.

[6]  A. Newen,et al.  Beyond the comparator model: A multifactorial two-step account of agency , 2008, Consciousness and Cognition.

[7]  M. Hallett,et al.  Neurology of volition , 2013, Experimental Brain Research.

[8]  P. Haggard,et al.  TMS stimulation over the inferior parietal cortex disrupts prospective sense of agency , 2014, Brain Structure and Function.

[9]  M. Nitsche,et al.  Safety criteria for transcranial direct current stimulation (tDCS) in humans , 2003, Clinical Neurophysiology.

[10]  R. Cardinal,et al.  ANOVA for the Behavioral Sciences Researcher , 2005 .

[11]  M. Jeannerod,et al.  Perception of self-generated movement following left parietal lesion. , 1999, Brain : a journal of neurology.

[12]  M. Brass,et al.  Feeling in control: Neural correlates of experience of agency , 2013, Cortex.

[13]  G. Cumming.  Understanding the Average Probability of Replication , 2005, Psychological science.

[14]  Sukhvinder S. Obhi,et al.  Intentional binding and the sense of agency: A review , 2012, Consciousness and Cognition.

[15]  Wolfgang Prinz,et al.  Action, binding and awareness , 2002 .

[16]  P. Haggard,et al.  Altered awareness of voluntary action after damage to the parietal cortex , 2004, Nature Neuroscience.

[17]  Hartwig R. Siebner,et al.  Cue integration and the perception of action in intentional binding , 2013, Experimental Brain Research.

[18]  D. Wolpert,et al.  Abnormalities in the awareness and control of action. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  B. Kloesel,et al.  Sequelae of a left-sided parietal stroke: Posterior alien hand syndrome , 2010, Neurocase.

[20]  Patrick Haggard,et al.  Agency, subjective time, and other minds. , 2007, Journal of experimental psychology. Human perception and performance.

[21]  A. Priori,et al.  Right but not left angular gyrus modulates the metric component of the mental body representation: a tDCS study , 2013, Experimental Brain Research.

[22]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

[23]  P. Haggard,et al.  Disrupting the experience of control in the human brain: pre-supplementary motor area contributes to the sense of agency , 2010, Proceedings of the Royal Society B: Biological Sciences.

[24]  P. Haggard,et al.  Awareness of action: Inference and prediction , 2008, Consciousness and Cognition.

[25]  V. Walsh,et al.  Transcranial Direct Current Stimulation Facilitates Decision Making in a Probabilistic Guessing Task , 2010, The Journal of Neuroscience.

[26]  A. Cravo,et al.  Voluntary action and causality in temporal binding , 2009, Experimental Brain Research.

[27]  Marc Jeannerod,et al.  Modulating the experience of agency: a positron emission tomography study , 2003, NeuroImage.

[28]  M. Brass,et al.  To Do or Not to Do: The Neural Signature of Self-Control , 2007, The Journal of Neuroscience.

[29]  P. Haggard,et al.  Experience of agency and sense of responsibility , 2011, Consciousness and Cognition.

[30]  ChrisD . Frith,et al.  Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia , 2009, Nature Reviews Neuroscience.

[31]  James R. Schott,et al.  Principles of Multivariate Analysis: A User's Perspective , 2002 .

[32]  Roy H. Hamilton,et al.  Space, time, and causality in the human brain , 2014, NeuroImage.

[33]  M. Koslowsky,et al.  tDCS polarity effects in motor and cognitive domains: a meta-analytical review , 2011, Experimental Brain Research.

[34]  C. Frith,et al.  Action, agency and responsibility , 2014, Neuropsychologia.

[35]  Woogul Lee,et al.  Self-determined, but not non-self-determined, motivation predicts activations in the anterior insular cortex: an fMRI study of personal agency. , 2013, Social cognitive and affective neuroscience.

[36]  N. Thakor,et al.  Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. , 1993, Electroencephalography and clinical neurophysiology.

[37]  A. Antal,et al.  Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients , 2007, Brain Research Bulletin.

[38]  L. Cohen,et al.  Transcranial direct current stimulation: State of the art 2008 , 2008, Brain Stimulation.

[39]  C. Plewnia,et al.  Shaping Memory Accuracy by Left Prefrontal Transcranial Direct Current Stimulation , 2014, The Journal of Neuroscience.

[40]  David J. Turk,et al.  The angular gyrus computes action awareness representations. , 2008, Cerebral cortex.

[41]  V. Walsh,et al.  Modulating Neuronal Activity Produces Specific and Long-Lasting Changes in Numerical Competence , 2010, Current Biology.

[42]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[43]  P. Fossati,et al.  Different brain structures related to self- and external-agency attribution: a brief review and meta-analysis , 2011, Brain Structure and Function.

[44]  P. Haggard,et al.  Exploring implicit and explicit aspects of sense of agency , 2012, Consciousness and Cognition.

[45]  James B. Rowe,et al.  Action selection: A race model for selected and non-selected actions distinguishes the contribution of premotor and prefrontal areas , 2010, NeuroImage.

[46]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[47]  M. Desmurget,et al.  Movement Intention After Parietal Cortex Stimulation in Humans , 2009, Science.

[48]  J. Marshall,et al.  The neural consequences of conflict between intention and the senses. , 1999, Brain : a journal of neurology.

[49]  P. Haggard,et al.  Voluntary action and conscious awareness , 2002, Nature Neuroscience.

[50]  M. Jeannerod,et al.  Awareness of action in schizophrenia , 2003, Neuroreport.

[51]  C. Marsden,et al.  Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. , 1995, Brain : a journal of neurology.

[52]  Ryota Kanai,et al.  Direct current stimulation (tDCS) reveals parietal asymmetry in local/global and salience-based selection , 2013, Cortex.

[53]  O. Carter,et al.  Evidence that transcranial direct current stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: A systematic review , 2015, Neuropsychologia.