Medicine:Error-related negativity

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Error-related negativity (ERN), sometimes referred to as the Ne, is a component of an event-related potential (ERP). ERPs are electrical activity in the brain as measured through electroencephalography (EEG) and time-locked to an external event (e.g., presentation of a visual stimulus) or a response (e.g. an error of commission). A robust ERN component is observed after errors are committed during various choice tasks, even when the participant is not explicitly aware of making the error;[1] however, in the case of unconscious errors the ERN is reduced.[2][3] An ERN is also observed when non-human primates commit errors.[4]

History

The ERN was first discovered in 1968 by Russian Natalia Petrovna Bekhtereva neuroscientist and psychologist and was called "error detector" [citation needed]. Later in 1990 ERN was developed by two independent research teams; Michael Falkenstein, J. Hohnsbein, J. Hoormann, & L. Blanke (1990) at the Institute for Work Physiology and Neurophysiology in Dortmund, Germany (who called it the "Ne"), and W.J. "Bill" Gehring, M.G.H. Coles, D.E. Meyer & E. Donchin (1990) at the University of Michigan, USA.[5][6] The ERN was observed in response to errors committed by study participants during simple choice response tasks.

Component characteristics

The ERN is a sharp negative going signal which begins about the same time an incorrect motor response begins, (response locked event-related potential), and typically peaks from 80 to 150 milliseconds (ms) after the erroneous response begins (or 40-80 ms after the onset of electromyographic activity).[7][8][9][10][11][2] The ERN is the largest at frontal and central electrode sites.[2] A typical method for determining the average ERN amplitude for an individual involves calculating the peak-to-peak difference in voltage between the average of the most negative peaks 1-150 ms after response onset, and the average amplitude of positive peaks 100-0 ms before response onset.[12] For optimal resolution of the signal, reference electrodes are typically placed behind both ears using either hardware or arithmetically linked mastoid electrodes.[8]

Main paradigms

Any paradigm in which mistakes are made during motor responses can be used to measure the ERN. Natural keyboarding is one such example where typing errors are shown to elicit ERN.[13] The most important feature of any ERN paradigm is obtaining a sufficient number of errors in the participant's responses, and the number of trials needed to obtain reliable scores can vary widely.[14] Early experiments identifying the component used a variety of techniques, including word and tone identification, and categorical discrimination (e.g. are the following an animal?).[6][15][16] However, the majority of experimental paradigms that elicit ERN deflections have been a variant on the Eriksen "Flanker",[12][17] and "Go/NoGo".[18] In addition to responses with the hands, the ERN can also be measured in paradigms where the task is performed with the feet[19] or with vocal responses as in the Stroop paradigm.[20]

A standard Flanker task involves discerning the central "target" letter from a string of distracting "flanker" letters which surround it. For example, congruous letter strings such as "SSSSS" or "HHHHH" and incongruous letter strings such as "HHSHH" or "SSHSS" may be presented on a computer screen. Each target letter would be assigned a key stroke response on a keyboard, such as "S" = right shift key and "H" = left shift key. Presentation of each letter string is brief, generally less than 100 ms, and central on the screen. Participants have approximately 2000 ms to respond before the next presentation. The most simple Go/NoGo tasks involve assigning a property of discernment to responding "Go" or not responding "NoGo." For example, again congruous letter strings such as "SSSSS" or "HHHHH" and incongruous letter strings such as "HHSHH" or "SSHSS" may be presented on a computer screen. The participant could be instructed to respond by pressing the space bar, only for congruous strings, and to not respond when presented with incongruous letter strings. More complicated Go/NoGo tasks are usually created when the ERN is the component of interest however, because in order to observe the robust negativity errors must be made. The classic Stroop paradigm involves a color-word task. Color words such as "red, yellow, orange, green" are presented centrally on a computer screen either in a color congruent with the word, ("red" in the color red) or in a color incongruent with the word ("red" in the color yellow). Participants may be asked to verbalize the color each word is written in. Incongruent and congruent presentations of the words can be manipulated to different rates, such as 25/75, 50/50, 30/70 etc.

Functional sensitivity

The amplitude of the ERN is sensitive to the intent and motivation of participants. When a participant is instructed to strive for accuracy in responses, observed amplitudes are typically larger than when participants are instructed to strive for speed.[12] Monetary incentives typically result in larger amplitudes as well.[21] Latency of the ERN peak amplitude can also vary between subjects, and does so reliably in special populations such as those diagnosed with ADHD, who show shorter latencies.[22] Participants with clinically diagnosed Obsessive Compulsive Disorder have exhibited ERN deflections with increased amplitude, prolonged latency, and a more posterior topography compared to clinically normal participants.[23][24][25] ERN latency has been manipulated through rapid feedback, wherein participants who received rapid feedback regarding the incorrect response subsequently showed shorter ERN peak latencies.[26] Additionally, a heightened ERN amplitude during social situations has been linked to anxiety symptoms in both childhood and adulthood.[27][28][29]

Developmental studies have shown that the ERN emerges throughout childhood and adolescence becoming more negative in amplitude and with a more defined peak.[30][31] The ERN appears to be modulated by the environment during childhood, with children who experience early adversity showing evidence of less negative ERN amplitudes.[31][32]

Theory/source

Although it is difficult to localize the origin of an ERP signal, extensive empirical research indicates that the ERN is most likely generated in the Anterior cingulate cortex (ACC) area of the brain. This conclusion is supported by fMRI,[33][34] and brain lesion research,[35] as well as dipole source modeling.[36] The Dorsolateral prefrontal cortex (DLPFC) may also be involved in the generation of the ERN to some degree, and it has been found that persons with higher levels of "absent-mindedness" have their ERN sourced more from that region.[37][38]

There is some debate within the field about what the ERN reflects (see especially Burle, et al.[39]) Some researchers maintain that the ERN is generated during the detection of or response to errors.[40][41] Others argue that the ERN is generated by a comparison process[11][39] or a conflict monitoring system,[42][43] and not specific to errors. In contrast to the above cognitive theories, new models suggest that the ERN may reflect the motivational significance of a task[44] or perhaps the emotional reaction to making an error.[45] This later view is consistent with findings linking errors and the ERN to autonomic arousal[46] and defensive motivated states,[47] and with findings suggesting that the ERN is dissociable from cognitive factors, but not affective ones.[45][48] Unfortunately, it is still unclear how to interpret differences in sizes of ERN, as both smaller and larger ERN have been interpreted as "better".[49]

Feedback error-related negativity

A stimulus locked event-related potential is also observed following the presentation of negative feedback stimuli in a cognitive task indicating the outcome of a response, often referred to as the feedback ERN (fERN).[50] This has led some researchers to extend the error-detection account of the response ERN (rERN) to a generic error detection system. This position has been elaborated into a reinforcement learning account of the ERN, arguing that both the rERN and the fERN are products of prediction error signals carried by the dopamine system arriving in the anterior cingulate cortex indicating that events have gone worse than expected.[51] In this framework it is common to measure both the rERN and the fERN as the difference in voltage between correct and incorrect responses and feedback, respectively.

Clinical applications

Debates about psychiatric disorders often become "chicken and egg" conundrums. The ERN has been proposed as a potential arbitrator of this argument. A body of empirical research has shown that the ERN reflects a "trait" level difference in individual error processing; especially concerning anxiety, rather than a "state" level difference.[21][52] For example; most people who experience depression do not feel depressed all of the time. Instead, they have periods of depressive "states" which may be minor and unique to an extreme situation such as death of a loved one, loss of employment, or major injury. However a person who has a depressive "trait" will have experienced more than one minor depressive "state" and usually at least one major depressive state, any of which may not be unique to an obviously extreme situation.[53] In fact, there is some evidence, albeit weak, that people with depression show small ERNs.[54][55] Scientists are exploring the use of the ERN and other ERP signals in identifying people at risk for psychiatric disorders in hopes of implementing early interventions. People with addictive behaviors such as smoking,[56] alcoholism,[57] and substance abuse[52] have also shown differential ERN responses compared to individuals without the same addictive behavior.

Pre-movement positivity

The ERN is often preceded by a small positive voltage deflection with a latency in the interval of -200 to -50 milliseconds in the response-locked ERP in channels over the scalp vertex, which is sometimes referred to as the "positive peak preceding the Ne" or "PNe",[58] but more generally thought to reflect the pre-movement positivity (PMP) described by Deecke et al. (1969).[59] The PMP is thought to reflect a "go signal" by which pre-SMA and SMA permit a motor response to be carried out.[60] PMP is smaller before error motor responses than it is before correct motor responses, suggesting that it may be an important signal for discriminating erroneous from correct actions. Additionally, PMP is smaller in people who make more mistakes during the Flankers task and may have clinical utility in accident prone populations, such as youths with ADHD.[61]

Error-related positivity

The ERN is often followed by a positivity, known as the error-related positivity or Pe. The Pe is a positive deflection with a centro-parietal distribution. When elicited, the Pe can occur 200-500ms after making an incorrect response, following the error negativity (Ne, ERN), but is not evident on all error trials.[11] In particular, the Pe is dependent on awareness or ability to detect errors.[1] Pe is basically the same as the P300 wave associated with conscious sensations.[62]:128 Additionally, Vocat et al. (2008)[63] established the Ne and Pe not only have different topographical distributions, but have different generators. Source localization indicates that the Ne has a dipole in the anterior cingulate cortex and the Pe has a dipole in the posterior cingulate cortex. The Pe amplitude reflects the perception of the error, meaning with more awareness of the error, the amplitude of the Pe is larger. Falkenstein and colleagues (2000) have shown that the Pe is elicited on uncorrected trials and false alarm trials, suggesting it is not directly related to error correction. It thus seems to be related to error monitoring, albeit with different neural and cognitive roots from the error-related processing reflected in the Ne.

If the Pe reflects conscious error processing, then it might be expected to be different for people with deficits in conflict monitoring, such as ADHD and OCD. Whether this is true remains controversial. Some studies do indicate these conditions are associated with different Pe responses,[64][65] whereas other studies have not replicated those findings.[66][67] The Pe has also been used to evaluate error processing in patients with severe brain traumatic injury. In a study using a variation of the Stroop task, patients with severe traumatic brain injury associated with deficits in error processing were found to show a significantly smaller Pe on error trials when compared against the healthy controls.[68]

Some researchers argue that error-related negativity or error-related positivity is in fact, reward-related positivity. Reward-related positivity is also referred to as reward positivity, or RewP.[69] It has been suggested that ERP data is depicting neural positivity to rewards (aka reward positivity) rather than neural negativity to loss (aka error-related negativity). Thus, this shift in how we conceptualize neural responses to gains/losses allows us to further understand the underlying neural processes.

See also


References

  1. ↑ 1.0 1.1 "Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task". Psychophysiology 38 (5): 752–60. September 2001. doi:10.1111/1469-8986.3850752. PMID 11577898. 
  2. ↑ 2.0 2.1 2.2 "Performance monitoring in a confusing world: error-related brain activity, judgments of response accuracy, and types of errors". Journal of Experimental Psychology. Human Perception and Performance 26 (1): 141–51. February 2000. doi:10.1037/0096-1523.26.1.141. PMID 10696610. 
  3. ↑ "Error awareness and the error-related negativity: evaluating the first decade of evidence". Frontiers in Human Neuroscience 6: 88. 2012. doi:10.3389/fnhum.2012.00088. PMID 22529791. 
  4. ↑ "Event-related potentials elicited by errors during the stop-signal task. I. Macaque monkeys". The Journal of Neuroscience 31 (44): 15640–9. November 2011. doi:10.1523/JNEUROSCI.3349-11.2011. PMID 22049407. 
  5. ↑ Gehring, William J.; Goss, Brian; Coles, Michael G. H.; Meyer, David E.; Donchin, Emanuel (2018-03-01). "The Error-Related Negativity" (in en). Perspectives on Psychological Science 13 (2): 200–204. doi:10.1177/1745691617715310. ISSN 1745-6916. PMID 29592655. https://doi.org/10.1177/1745691617715310. 
  6. ↑ 6.0 6.1 "The error-related negativity: an event-related brain potential accompanying errors". Psychophysiology 27: 34. 1990. 
  7. ↑ Gehring WJ (1993). The error-related negativity: Evidence for a neural mechanism for error-related processing (Ph.D. thesis). University of Illinois at Urbana-Champaign.
  8. ↑ 8.0 8.1 "A neural system for error detection and compensation". Psychological Science 4 (6): 385–390. 1993. doi:10.1111/j.1467-9280.1993.tb00586.x. 
  9. ↑ "Error monitoring during reward and avoidance learning in high- and low-socialized individuals". Psychophysiology 37 (1): 43–54. January 2000. doi:10.1111/1469-8986.3710043. PMID 10705766. 
  10. ↑ "Medial frontal cortex in action monitoring". The Journal of Neuroscience 20 (1): 464–9. January 2000. doi:10.1523/JNEUROSCI.20-01-00464.2000. PMID 10627622. 
  11. ↑ 11.0 11.1 11.2 "ERP components on reaction errors and their functional significance: a tutorial". Biological Psychology 51 (2–3): 87–107. January 2000. doi:10.1016/S0301-0511(99)00031-9. PMID 10686361. 
  12. ↑ 12.0 12.1 12.2 "Dissociable medial frontal negativities from a common monitoring system for self- and externally caused failure of goal achievement". NeuroImage 47 (4): 2023–30. October 2009. doi:10.1016/j.neuroimage.2009.05.064. PMID 19486945. 
  13. ↑ Kalfaoglu, C; Stafford, T; Milne, L (2018). "Frontal theta band oscillations predict error correction and post-error slowing in typing.". Journal of Experimental Psychology: Human Perception and Performance 44 (1): 69–88. doi:10.1037/xhp0000417. PMID 28447844. http://eprints.whiterose.ac.uk/112945/1/JEP_HPP_MS_accepted.pdf. 
  14. ↑ Clayson, Peter E. (2020). "Moderators of the internal consistency of error-related negativity scores: A meta-analysis of internal consistency estimates" (in en). Psychophysiology 57 (8): e13583. doi:10.1111/psyp.13583. ISSN 1469-8986. PMID 32324305. https://onlinelibrary.wiley.com/doi/abs/10.1111/psyp.13583. 
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  19. ↑ "Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans". Neuroscience Letters 242 (2): 65–8. February 1998. doi:10.1016/S0304-3940(98)00035-4. PMID 9533395. 
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  21. ↑ 21.0 21.1 "The error-related negativity as a state and trait measure: motivation, personality, and ERPs in response to errors". Psychophysiology 41 (1): 84–95. January 2004. doi:10.1111/1469-8986.00124. PMID 14693003. http://www.science.mcmaster.ca/pnb/department/seminars/readings/Pailing%20%26%20Segalowitz%20(2004).pdf. 
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  23. ↑ "Discrepant target detection and action monitoring in obsessive-compulsive disorder". Psychiatry Research 108 (2): 101–10. November 2001. doi:10.1016/S0925-4927(01)00117-2. PMID 11738544. 
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  38. ↑ "Individual differences discriminate event-related potentials but not performance during response inhibition". Experimental Brain Research 160 (1): 60–70. January 2005. doi:10.1007/s00221-004-1985-z. PMID 15480606. 
  39. ↑ 39.0 39.1 "Error negativity does not reflect conflict: a reappraisal of conflict monitoring and anterior cingulate cortex activity". Journal of Cognitive Neuroscience 20 (9): 1637–55. September 2008. doi:10.1162/jocn.2008.20110. PMID 18345992. 
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  41. ↑ "Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing". Biological Psychology 56 (3): 173–89. June 2001. doi:10.1016/s0301-0511(01)00076-x. PMID 11399349. 
  42. ↑ Larson, Michael J.; Clayson, Peter E.; Clawson, Ann (2014-09-01). "Making sense of all the conflict: A theoretical review and critique of conflict-related ERPs" (in en). International Journal of Psychophysiology 93 (3): 283–297. doi:10.1016/j.ijpsycho.2014.06.007. ISSN 0167-8760. PMID 24950132. https://www.sciencedirect.com/science/article/abs/pii/S016787601400141X. 
  43. ↑ "Conflict monitoring and anterior cingulate cortex: an update". Trends in Cognitive Sciences 8 (12): 539–46. December 2004. doi:10.1016/j.tics.2004.10.003. PMID 15556023. 
  44. ↑ "On the ERN and the significance of errors". Psychophysiology 42 (2): 151–60. March 2005. doi:10.1111/j.1469-8986.2005.00270.x. PMID 15787852. 
  45. ↑ 45.0 45.1 "ERN and the placebo: a misattribution approach to studying the arousal properties of the error-related negativity". Journal of Experimental Psychology. General 141 (4): 799–807. November 2012. doi:10.1037/a0027586. PMID 22390264. 
  46. ↑ "To err is autonomic: error-related brain potentials, ANS activity, and post-error compensatory behavior". Psychophysiology 40 (6): 895–903. November 2003. doi:10.1111/1469-8986.00107. PMID 14986842. 
  47. ↑ "Errors are aversive: defensive motivation and the error-related negativity". Psychological Science 19 (2): 103–8. February 2008. doi:10.1111/j.1467-9280.2008.02053.x. PMID 18271855. 
  48. ↑ "Alcohol effects on performance monitoring and adjustment: affect modulation and impairment of evaluative cognitive control". Journal of Abnormal Psychology 121 (1): 173–86. February 2012. doi:10.1037/a0023664. PMID 21604824. 
  49. ↑ Clayson, Peter E.; Kappenman, Emily S.; Gehring, William J.; Miller, Gregory A.; Larson, Michael J. (2021-07-01). "A commentary on establishing norms for error-related brain activity during the arrow flanker task among young adults" (in en). NeuroImage 234: 117932. doi:10.1016/j.neuroimage.2021.117932. ISSN 1053-8119. PMID 33677074. 
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  51. ↑ "The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity". Psychological Review 109 (4): 679–709. October 2002. doi:10.1037/0033-295x.109.4.679. PMID 12374324. 
  52. ↑ 52.0 52.1 "The error-related negativity (ERN) and psychopathology: toward an endophenotype". Clinical Psychology Review 28 (8): 1343–54. December 2008. doi:10.1016/j.cpr.2008.07.003. PMID 18694617. 
  53. ↑ "Population-based study of first onset and chronicity in major depressive disorder". Archives of General Psychiatry 65 (5): 513–20. May 2008. doi:10.1001/archpsyc.65.5.513. PMID 18458203. 
  54. ↑ Moran, Tim P.; Schroder, Hans S.; Kneip, Chelsea; Moser, Jason S. (2017-01-01). "Meta-analysis and psychophysiology: A tutorial using depression and action-monitoring event-related potentials" (in en). International Journal of Psychophysiology. Rigor and Replication: Towards Improved Best Practices in Psychophysiological Research 111: 17–32. doi:10.1016/j.ijpsycho.2016.07.001. ISSN 0167-8760. PMID 27378538. http://www.sciencedirect.com/science/article/pii/S0167876016301222. 
  55. ↑ Clayson, Peter E.; Carbine, Kaylie A.; Larson, Michael J. (2020-04-01). "A registered report of error-related negativity and reward positivity as biomarkers of depression: P-Curving the evidence" (in en). International Journal of Psychophysiology 150: 50–72. doi:10.1016/j.ijpsycho.2020.01.005. ISSN 0167-8760. PMID 31987869. http://www.sciencedirect.com/science/article/pii/S0167876020300180. 
  56. ↑ "Evidence for a deficit in the salience attribution to errors in smokers". Drug and Alcohol Dependence 106 (2–3): 181–5. January 2010. doi:10.1016/j.drugalcdep.2009.08.014. PMID 19781864. 
  57. ↑ "Smaller feedback ERN amplitudes during the BART are associated with a greater family history density of alcohol problems in treatment-naïve alcoholics". Drug and Alcohol Dependence 92 (1–3): 141–8. January 2008. doi:10.1016/j.drugalcdep.2007.07.017. PMID 17869027. 
  58. ↑ "Action monitoring in boys with attention-deficit/hyperactivity disorder, their nonaffected siblings, and normal control subjects: evidence for an endophenotype". Biological Psychiatry 64 (7): 615–625. 2008. doi:10.1016/j.biopsych.2007.12.016. PMID 18339358. 
  59. ↑ "Distribution of readiness potential, pre-motion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements". Experimental Brain Research 7 (2): 158–168. 1969. doi:10.1007/BF00235441. PMID 5799432. 
  60. ↑ "Pre-motion positivity during self-paced movements of finger and mouth". NeuroReport 17 (9): 883–886. 2006. doi:10.1097/01.wnr.0000221830.95598.ea. PMID 16738481. 
  61. ↑ "Reduced premovement positivity during the stimulus-response interval precedes errors: using single-trial and regression ERPs to understand performance deficits in ADHD". Psychophysiology 56 (9): e13392. 2019. doi:10.1111/psyp.13392. PMID 31081153. 
  62. ↑ Dehaene, Stanislas (2014). Consciousness and the Brain: Deciphering How the Brain Codes Our Thoughts. Viking. ISBN 978-0670025435. 
  63. ↑ "Unavoidable errors: a spatio-temporal analysis of time-course and neural sources of evoked potentials associated with error processing in a speeded task". Neuropsychologia 46 (10): 2545–55. August 2008. doi:10.1016/j.neuropsychologia.2008.04.006. PMID 18533202. 
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  65. ↑ "Error-related electrocortical responses are enhanced in children with obsessive-compulsive behaviors". Developmental Neuropsychology 29 (3): 431–45. 2006. doi:10.1207/s15326942dn2903_3. PMID 16671860. 
  66. ↑ "Neural activity associated with executive functions in adolescents with attention-deficit/hyperactivity disorder (ADHD)". International Journal of Psychophysiology 74 (1): 19–27. October 2009. doi:10.1016/j.ijpsycho.2009.06.003. PMID 19607863. https://duepublico2.uni-due.de/servlets/MCRFileNodeServlet/duepublico_derivate_00028098/Oades2009Neural.pdf. 
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  69. ↑ Proudfit, Greg Hajcak (April 2015). "The reward positivity: From basic research on reward to a biomarker for depression: The reward positivity". Psychophysiology 52 (4): 449–459. doi:10.1111/psyp.12370. PMID 25327938. 



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