Development of ERN together with an internal model of audio-motor associations

The brain's reactions to error are manifested in several event related potentials (ERP) components, derived from electroencephalographic (EEG) signals. Although these components have been known for decades, their interpretation is still controversial. A current hypothesis (first indicator hypothesis) claims that the first indication of an action being erroneous leads to a negative deflection of the EEG signal over frontal midline areas. In some cases this requires sensory feedback in the form of knowledge of results (KR). If KR is given, then the first negative deflection can be found around 250 ms after feedback presentation (feedback-related negativity, FRN). When KR is not required, a negative deflection is found already around 100 ms after action onset (ERN). This deflection may be evoked when a mismatch between required and actually executed actions is detected. To detect such a mismatch, however, necessitates knowledge about which action is required. To test this assumption, the current study monitored EEG error components during acquisition of an internal model, i.e., acquisition of the knowledge of which actions are needed to reach certain goals. Actions consisted of finger presses on a piano keyboard and goals were tones of a certain pitch to be generated, thus the internal model represented audio-motor mapping. Results show that with increasing proficiency in mapping goals to appropriate actions, the amplitude of the ERN increased, whereas the amplitude of the FRN remained unchanged. Thus, when knowledge is present about which action is required, this supports generation of an ERN around 100 ms, likely by detecting a mismatch between required and performed actions. This is in accordance with the first indicator hypothesis. The present study furthermore lends support to the notion that FRN mainly relies on comparison of sensory targets with sensory feedback.

[1]  L. Jäncke,et al.  A Network for Sensory‐Motor Integration , 2005, Annals of the New York Academy of Sciences.

[2]  Jutta Stahl,et al.  Error detection and the use of internal and external error indicators: an investigation of the first-indicator hypothesis. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[3]  Eckart Altenmüller,et al.  Annals of the New York Academy of Sciences the Involvement of Audio–motor Coupling in the Music-supported Therapy Applied to Stroke Patients , 2022 .

[4]  A. Rodríguez-Fornells,et al.  What the brain does before the tongue slips. , 2006, Cerebral cortex.

[5]  R. Näätänen,et al.  The mismatch negativity (MMN) in basic research of central auditory processing: A review , 2007, Clinical Neurophysiology.

[6]  Peter Ullsperger,et al.  Dissociable medial frontal negativities from a common monitoring system for self- and externally caused failure of goal achievement , 2009, NeuroImage.

[7]  Daniel M. Wolpert,et al.  Forward Models for Physiological Motor Control , 1996, Neural Networks.

[8]  Clay B. Holroyd,et al.  Hierarchical error processing: Different errors, different systems , 2007, Brain Research.

[9]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[10]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[11]  Wolzt,et al.  World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. , 2003, The Journal of the American College of Dentists.

[12]  Clay B. Holroyd,et al.  Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals , 2004, Nature Neuroscience.

[13]  A. Rodríguez-Fornells,et al.  Brain potentials related to self-generated and external information used for performance monitoring , 2005, Clinical Neurophysiology.

[14]  J. Hohnsbein,et al.  Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. , 1991, Electroencephalography and clinical neurophysiology.

[15]  D. Meyer,et al.  A Neural System for Error Detection and Compensation , 1993 .

[16]  Clay B. Holroyd,et al.  Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing , 2001, Biological Psychology.

[17]  D. Tucker,et al.  Electrophysiological Responses to Errors and Feedback in the Process of Action Regulation , 2003, Psychological science.

[18]  R. Baker,et al.  When is an error not a prediction error? An electrophysiological investigation , 2009, Cognitive, affective & behavioral neuroscience.

[19]  D. V. von Cramon,et al.  Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging , 2003, The Journal of Neuroscience.

[20]  María Herrojo Ruiz,et al.  Detecting wrong notes in advance: neuronal correlates of error monitoring in pianists. , 2009, Cerebral cortex.

[21]  Thomas F Münte,et al.  Coupling electrophysiological and hemodynamic responses to errors , 2012, Human brain mapping.

[22]  Lutz Jäncke,et al.  Motor and non-motor error and the influence of error magnitude on brain activity , 2010, Experimental Brain Research.

[23]  N. Yeung,et al.  Decision Processes in Human Performance Monitoring , 2010, The Journal of Neuroscience.

[24]  Christiane,et al.  World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. , 2004, Journal international de bioethique = International journal of bioethics.

[25]  D. V. Cramon,et al.  Subprocesses of Performance Monitoring: A Dissociation of Error Processing and Response Competition Revealed by Event-Related fMRI and ERPs , 2001, NeuroImage.

[26]  Robert Leech,et al.  Distinct frontal networks are involved in adapting to internally and externally signaled errors. , 2013, Cerebral cortex.

[27]  Thomas F Münte,et al.  Internal and external information in error processing , 2008, BMC Neuroscience.

[28]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[29]  Conny F. Schmidt,et al.  A network for audio–motor coordination in skilled pianists and non-musicians , 2007, Brain Research.

[30]  C. Braun,et al.  Event-Related Brain Potentials Following Incorrect Feedback in a Time-Estimation Task: Evidence for a Generic Neural System for Error Detection , 1997, Journal of Cognitive Neuroscience.

[31]  L. Jäncke The dynamic audio–motor system in pianists , 2012, Annals of the New York Academy of Sciences.

[32]  Emanuel Donchin,et al.  Neural response to action and reward prediction errors: Comparing the error-related negativity to behavioral errors and the feedback-related negativity to reward prediction violations. , 2011, Psychophysiology.

[33]  Jonathan D. Cohen,et al.  The neural basis of error detection: conflict monitoring and the error-related negativity. , 2004, Psychological review.

[34]  R. Näätänen The Mismatch Negativity: A Powerful Tool for Cognitive Neuroscience , 1995, Ear and hearing.

[35]  Stefan Koelsch,et al.  Processing Expectancy Violations during Music Performance and Perception: An ERP Study , 2010, Journal of Cognitive Neuroscience.

[36]  Karl Theodor Kalveram,et al.  The inverse problem in cognitive, perceptual, and proprioceptive control of sensorimotor behaviour: Towards a biologically plausible model of the control of aiming movements , 2004 .

[37]  K. Alho Cerebral Generators of Mismatch Negativity (MMN) and Its Magnetic Counterpart (MMNm) Elicited by Sound Changes , 1995, Ear and hearing.

[38]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.