Abstract
The error-related negativity (ERN) is a neural correlate of error monitoring often used to investigate individual differences in developmental, mental health, and adaptive contexts. However, limited experimental control over errors presents several confounds to its measurement. An experimentally controlled disturbance to standing balance evokes the balance N1, which we previously suggested may share underlying mechanisms with the ERN based on a number of shared features and factors. We now measure whether the balance N1 and ERN are correlated across individuals within two small groups (N = 21 young adults and N = 20 older adults). ERNs were measured in arrow flanker tasks using hand and foot response modalities (ERN-hand and ERN-foot). The balance N1 was evoked by sudden slip-like movements of the floor while standing. The ERNs and the balance N1 showed good and excellent internal consistency, respectively, and were correlated in amplitude in both groups. One principal component strongly loaded on all three evoked potentials, suggesting that the majority of individual differences are shared across the three ERPs. However, there remains a significant component of variance shared between the ERN-hand and ERN-foot beyond what they share with the balance N1. It is unclear whether this component of variance is specific to the arrow flanker task, or something fundamentally related to error processing that is not evoked by a sudden balance disturbance. If the balance N1 were to reflect error processing mechanisms indexed by the ERN, balance paradigms offer several advantages in terms of experimental control over errors.
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Data availability
MATLAB datasets containing all of the analyzed subject-averaged EEG waveforms are available at https://github.com/AidenPayne/ERN-n1-2023.
References
Ackermann H, Diener HC, Dichgans J (1986) Mechanically evoked cerebral potentials and long-latency muscle responses in the evaluation of afferent and efferent long-loop pathways in humans. Neurosci Lett 66:233–238. https://doi.org/10.1016/0304-3940(86)90024-8
Adkin AL, Quant S, Maki BE, McIlroy WE (2006) Cortical responses associated with predictable and unpredictable compensatory balance reactions. Exp Brain Res 172:85–93. https://doi.org/10.1007/s00221-005-0310-9
Adkin AL, Campbell AD, Chua R, Carpenter MG (2008) The influence of postural threat on the cortical response to unpredictable and predictable postural perturbations. Neurosci Lett 435:120–125. https://doi.org/10.1016/j.neulet.2008.02.018
Balaban CD (2002) Neural substrates linking balance control and anxiety. Physiol Behav 77:469–475. https://doi.org/10.1016/S0031-9384(02)00935-6
Balaban CD, Thayer JF (2001) Neurological bases for balance-anxiety links. J Anxiety Disord 15:53–79. https://doi.org/10.1016/S0887-6185(00)00042-6
Bart O, Bar-Haim Y, Weizman E, Levin M, Sadeh A, Mintz M (2009) Balance treatment ameliorates anxiety and increases self-esteem in children with comorbid anxiety and balance disorder. Res Dev Disabil 30:486–495. https://doi.org/10.1016/j.ridd.2008.07.008
Berger W, Quintern J, Dietz V (1987) Afferent and efferent control of stance and gait: developmental changes in children. Electroencephalogr Clin Neurophysiol 66:244–252. https://doi.org/10.1016/0013-4694(87)90073-3
Berger W, Horstmann GA, Dietz V (1990) Interlimb coordination of stance in children: divergent modulation of spinal reflex responses and cerebral evoked potentials in terms of age. Neurosci Lett 116:118–122
Bernstein PS, Scheffers MK, Coles MGH (1995) “Where did I go wrong?” A psychophysiological analysis of error detection. J Exp Psychol Hum Percept Perform 21:1312–1322. https://doi.org/10.1037/0096-1523.21.6.1312
Beste C, Dziobek I, Hielscher H, Willemssen R, Falkenstein M (2009a) Effects of stimulus-response compatibility on inhibitory processes in Parkinson’s disease. Eur J Neurosci 29:855–860. https://doi.org/10.1111/j.1460-9568.2009.06621.x
Beste C, Willemssen R, Saft C, Falkenstein M (2009b) Error processing in normal aging and in basal ganglia disorders. Neuroscience 159:143–149. https://doi.org/10.1016/j.neuroscience.2008.12.030
Bolmont B, Gangloff P, Vouriot A, Perrin PP (2002) Mood states and anxiety influence abilities to maintain balance control in healthy human subjects. Neurosci Lett 329:96–100. https://doi.org/10.1016/S0304-3940(02)00578-5
Bonini F, Burle B, Liegeois-Chauvel C, Regis J, Chauvel P, Vidal F (2014) Action monitoring and medial frontal cortex: leading role of supplementary motor area. Science 343:888–891. https://doi.org/10.1126/science.1247412
Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4:215–222. https://doi.org/10.1016/s1364-6613(00)01483-2
Cassidy SM, Robertson IH, O’Connell RG (2012) Retest reliability of event-related potentials: evidence from a variety of paradigms. Psychophysiology 49:659–664. https://doi.org/10.1111/j.1469-8986.2011.01349.x
Dehaene S, Posner M, Tucker D (1994) Localization of a neural system for error detection and compensation. Psychol Sci. https://doi.org/10.1111/j.1467-9280.1994.tb00630.x
Dietz V, Quintern J, Berger W (1985) Afferent control of human stance and gait: evidence for blocking of group I afferents during gait. Exp Brain Res 61:153–163. https://doi.org/10.1007/BF00235630
Ditz JC, Schwarz A, Muller-Putz GR (2020) Perturbation-evoked potentials can be classified from single-trial EEG. J Neural Eng 17:036008. https://doi.org/10.1088/1741-2552/ab89fb
Duckrow RB, Abu-Hasaballah K, Whipple R, Wolfson L (1999) Stance perturbation-evoked potentials in old people with poor gait and balance. Clin Neurophysiol 110:2026–2032. https://doi.org/10.1016/S1388-2457(99)00195-9
Eriksen BA, Eriksen CW (1974) Effects of noise letters upon the identification of a target letter in a nonsearch task*. Percept Psychophys 16:143–149
Fischer AG, Klein TA, Ullsperger M (2017) Comparing the error-related negativity across groups: the impact of error- and trial-number differences. Psychophysiology 54:998–1009. https://doi.org/10.1111/psyp.12863
Gallea C, Graaf JB, Pailhous J, Bonnard M (2008) Error processing during online motor control depends on the response accuracy. Behav Brain Res 193:117–125. https://doi.org/10.1016/j.bbr.2008.05.014
Gehring WJ, Goss B, Coles MGH, Meyer DE, Donchin E (1993) A neural system for error-detection and compensation. Psychol Sci 4:385–390. https://doi.org/10.1111/j.1467-9280.1993.tb00586.x
Gentsch A, Ullsperger P, Ullsperger M (2009) Dissociable medial frontal negativities from a common monitoring system for self- and externally caused failure of goal achievement. Neuroimage 47:2023–2030. https://doi.org/10.1016/j.neuroimage.2009.05.064
Gratton G, Coles MG, Donchin E (1983) A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 55:468–484. https://doi.org/10.1016/0013-4694(83)90135-9
Hajcak G, Moser JS, Yeung N, Simons RF (2005) On the ERN and the significance of errors. Psychophysiology 42:151–160. https://doi.org/10.1111/j.1469-8986.2005.00270.x
Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG (2009) Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 42:377–381. https://doi.org/10.1016/j.jbi.2008.08.010
Harris PA, Taylor R, Minor BL et al (2019) The REDCap consortium: building an international community of software platform partners. J Biomed Inform 95:103208. https://doi.org/10.1016/j.jbi.2019.103208
Holroyd CB, Coles MG (2002) The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 109:679–709. https://doi.org/10.1037/0033-295x.109.4.679
Holroyd CB, Dien J, Coles MG (1998) Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans. Neurosci Lett 242:65–68. https://doi.org/10.1016/S0304-3940(98)00035-4
Horak FB, Nashner LM (1986) Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 55:1369–1381. https://doi.org/10.1152/jn.1986.55.6.1369
Jacobs JV, Horak FB (2007) Cortical control of postural responses. J Neural Transm (vienna) 114:1339–1348. https://doi.org/10.1007/s00702-007-0657-0
Jacob RG, Woody SR, Clark DB et al (1997) Discomfort with space and motion: a possible marker of vestibular dysfunction assessed by the situational characteristics questionnaire. J Psychopathol Behav Assess 15:299–324
Kim EY, Iwaki N, Uno H, Fujita T (2005) Error-related negativity in children: effect of an observer. Dev Neuropsychol 28:871–883. https://doi.org/10.1207/s15326942dn2803_7
Klawohn J, Endrass T, Preuss J, Riesel A, Kathmann N (2016) Modulation of hyperactive error signals in obsessive-compulsive disorder by dual-task demands. J Abnorm Psychol 125:292–298. https://doi.org/10.1037/abn0000134
Lewis MD, Stieben J (2004) Emotion regulation in the brain: conceptual issues and directions for developmental research. Child Dev 75:371–376. https://doi.org/10.1111/j.1467-8624.2004.00680.x
Little CE, Woollacott M (2015) EEG measures reveal dual-task interference in postural performance in young adults. Exp Brain Res 233:27–37. https://doi.org/10.1007/s00221-014-4111-x
LoTemplio SB, Lopes CL, McDonnell AS, Scott EE, Payne BR, Strayer DL (2023) Updating the relationship of the Ne/ERN to task-related behavior: a brief review and suggestions for future research. Front Hum Neurosci 17:1150244. https://doi.org/10.3389/fnhum.2023.1150244
Luu P, Tucker DM, Makeig S (2004) Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation. Clin Neurophysiol 115:1821–1835. https://doi.org/10.1016/j.clinph.2004.03.031
Marlin A, Mochizuki G, Staines WR, McIlroy WE (2014) Localizing evoked cortical activity associated with balance reactions: does the anterior cingulate play a role? J Neurophysiol 111:2634–2643. https://doi.org/10.1152/jn.00511.2013
Maurer LK, Maurer H, Muller H (2015) Neural correlates of error prediction in a complex motor task. Front Behav Neurosci 9:209. https://doi.org/10.3389/fnbeh.2015.00209
Meyer A, Hajcak G, Torpey DC et al (2013a) Increased error-related brain activity in six-year-old children with clinical anxiety. J Abnorm Child Psychol 41:1257–1266. https://doi.org/10.1007/s10802-013-9762-8
Meyer A, Riesel A, Proudfit GH (2013b) Reliability of the ERN across multiple tasks as a function of increasing errors. Psychophysiology 50:1220–1225. https://doi.org/10.1111/psyp.12132
Meyer A, Bress JN, Proudfit GH (2014) Psychometric properties of the error-related negativity in children and adolescents. Psychophysiology 51:602–610. https://doi.org/10.1111/psyp.12208
Meyer A, Lerner MD, De Los RA, Laird RD, Hajcak G (2017) Considering ERP difference scores as individual difference measures: Issues with subtraction and alternative approaches. Psychophysiology 54:114–122. https://doi.org/10.1111/psyp.12664
Mierau A, Hulsdunker T, Struder HK (2015) Changes in cortical activity associated with adaptive behavior during repeated balance perturbation of unpredictable timing. Front Behav Neurosci 9:272. https://doi.org/10.3389/fnbeh.2015.00272
Mochizuki G, Sibley KM, Cheung HJ, Camilleri JM, McIlroy WE (2009a) Generalizability of perturbation-evoked cortical potentials: Independence from sensory, motor and overall postural state. Neurosci Lett 451:40–44. https://doi.org/10.1016/j.neulet.2008.12.020
Mochizuki G, Sibley KM, Cheung HJ, McIlroy WE (2009b) Cortical activity prior to predictable postural instability: is there a difference between self-initiated and externally-initiated perturbations? Brain Res 1279:29–36. https://doi.org/10.1016/j.brainres.2009.04.050
Mochizuki G, Boe S, Marlin A, McIlRoy WE (2010) Perturbation-evoked cortical activity reflects both the context and consequence of postural instability. Neuroscience 170:599–609. https://doi.org/10.1016/j.neuroscience.2010.07.008
Moser JS, Moran TP, Schroder HS, Donnellan MB, Yeung N (2013) On the relationship between anxiety and error monitoring: a meta-analysis and conceptual framework. Front Hum Neurosci 7:466. https://doi.org/10.3389/fnhum.2013.00466
Nieuwenhuis S, Ridderinkhof KR, Talsma D, Coles MG, Holroyd CB, Kok A, van der Molen MW (2002) A computational account of altered error processing in older age: dopamine and the error-related negativity. Cogn Affect Behav Neurosci 2:19–36. https://doi.org/10.3758/CABN.2.1.19
Notebaert W, Houtman F, Opstal FV, Gevers W, Fias W, Verguts T (2009) Post-error slowing: an orienting account. Cognition 111:275–279. https://doi.org/10.1016/j.cognition.2009.02.002
Olvet DM, Hajcak G (2008) The error-related negativity (ERN) and psychopathology: toward an endophenotype. Clin Psychol Rev 28:1343–1354. https://doi.org/10.1016/j.cpr.2008.07.003
Payne AM, Ting LH (2020a) Worse balance is associated with larger perturbation-evoked cortical responses in healthy young adults. Gait Posture 80:324–330. https://doi.org/10.1016/j.gaitpost.2020.06.018
Payne AM, Ting LH (2020b) Balance perturbation-evoked cortical N1 responses are larger when stepping and not influenced by motor planning. J Neurophysiol 124:1875–1884. https://doi.org/10.1152/jn.00341.2020
Payne AM, Hajcak G, Ting LH (2019a) Dissociation of muscle and cortical response scaling to balance perturbation acceleration. J Neurophysiol 121:867–880. https://doi.org/10.1152/jn.00237.2018
Payne AM, Ting LH, Hajcak G (2019b) Do sensorimotor perturbations to standing balance elicit an error-related negativity? Psychophysiology. https://doi.org/10.1111/psyp.13359
Payne AM, Palmer JA, McKay JL, Ting LH (2021) Lower cognitive set shifting ability is associated with stiffer balance recovery behavior and larger perturbation-evoked cortical responses in older adults. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2021.742243
Payne AM, McKay JL, Ting LH (2022) The cortical N1 response to balance perturbation is associated with balance and cognitive function in different ways between older adults with and without Parkinson’s disease. Cerebr Cortex Commun. https://doi.org/10.1093/texcom/tgac030
Payne AM, Ting LH, Hajcak G (2023) The balance N1 and the ERN correlate in amplitude across individuals in small samples of younger and older adults. bioRxiv. https://doi.org/10.1101/2022.09.16.508295
Peterson SM, Ferris DP (2018) Differentiation in theta and beta electrocortical activity between visual and physical perturbations to walking and standing balance. eNeuro. https://doi.org/10.1523/ENEURO.0207-18.2018
Peterson SM, Ferris DP (2019) Group-level cortical and muscular connectivity during perturbations to walking and standing balance. Neuroimage 198:93–103. https://doi.org/10.1016/j.neuroimage.2019.05.038
Quant S, Adkin AL, Staines WR, Maki BE, McIlroy WE (2004) The effect of a concurrent cognitive task on cortical potentials evoked by unpredictable balance perturbations. BMC Neurosci 5:1–12. https://doi.org/10.1186/1471-2202-5-18
Quintern J, Berger W, Dietz V (1985) Compensatory reactions to gait perturbations in man: short- and long-term effects of neuronal adaptation. Neurosci Lett 62:371–376
Riesel A, Weinberg A, Endrass T, Meyer A, Hajcak G (2013) The ERN is the ERN is the ERN? Convergent validity of error-related brain activity across different tasks. Biol Psychol 93:377–385. https://doi.org/10.1016/j.biopsycho.2013.04.007
Schmid G, Henningsen P, Dieterich M, Sattel H, Lahmann C (2011) Psychotherapy in dizziness: a systematic review. J Neurol Neurosurg Psychiatry 82:601–606. https://doi.org/10.1136/jnnp.2010.237388
Seer C, Lange F, Georgiev D, Jahanshahi M, Kopp B (2016) Event-related potentials and cognition in Parkinson’s disease: an integrative review. Neurosci Biobehav Rev 71:691–714. https://doi.org/10.1016/j.neubiorev.2016.08.003
Sibley KM, Mochizuki G, Frank JS, McIlroy WE (2010) The relationship between physiological arousal and cortical and autonomic responses to postural instability. Exp Brain Res 203:533–540. https://doi.org/10.1007/s00221-010-2257-8
Staines WR, McIlroy WE, Brooke JD (2001) Cortical representation of whole-body movement is modulated by proprioceptive discharge in humans. Exp Brain Res 138:235–242. https://doi.org/10.1007/s002210100691
Tamnes CK, Walhovd KB, Torstveit M, Sells VT, Fjell AM (2013) Performance monitoring in children and adolescents: a review of developmental changes in the error-related negativity and brain maturation. Dev Cogn Neurosci 6:1–13. https://doi.org/10.1016/j.dcn.2013.05.001
Themanson JR, Hillman CH (2006) Cardiorespiratory fitness and acute aerobic exercise effects on neuroelectric and behavioral measures of action monitoring. Neuroscience 141:757–767. https://doi.org/10.1016/j.neuroscience.2006.04.004
Ullsperger M, Danielmeier C, Jocham G (2014) Neurophysiology of performance monitoring and adaptive behavior. Physiol Rev 94:35–79. https://doi.org/10.1152/physrev.00041.2012
Van der Borght L, Houtman F, Burle B, Notebaert W (2016) Distinguishing the influence of task difficulty on error-related ERPs using surface Laplacian transformation. Biol Psychol 115:78–85. https://doi.org/10.1016/j.biopsycho.2016.01.013
Van’t Ent D, Apkarian P (1999) Motoric response inhibition in finger movement and saccadic eye movement: a comparative study. Clin Neurophysiol 110:1058–1072. https://doi.org/10.1016/S1388-2457(98)00036-4
Varghese JP, Marlin A, Beyer KB, Staines WR, Mochizuki G, McIlroy WE (2014) Frequency characteristics of cortical activity associated with perturbations to upright stability. Neurosci Lett 578:33–38. https://doi.org/10.1016/j.neulet.2014.06.017
Warrens MJ (2017) Transforming intraclass correlation coefficients with the Spearman-Brown formula. J Clin Epidemiol 85:14–16. https://doi.org/10.1016/j.jclinepi.2017.03.005
Welch TD, Ting LH (2014) Mechanisms of motor adaptation in reactive balance control. PLoS ONE 9:e96440. https://doi.org/10.1371/journal.pone.0096440
Wessel JR (2018) An adaptive orienting theory of error processing. Psychophysiology. https://doi.org/10.1111/psyp.13041
Yardley L, Redfern MS (2001) Psychological factors influencing recovery from balance disorders. J Anxiety Disord 15:107–119. https://doi.org/10.1016/S0887-6185(00)00045-1
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This work was supported by the National Institutes of Health (F32 MH129076, P50 NS098685, R21 HD075612, R01 HD46922, UL1 TR000424), National Science Foundation (EFRI 1137229), the Fulton County Elder Health Scholarship (2015 -2017), and the Zebrowitz Award (2018).
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LHT provided funding; AMP, LHT, and GH were involved in the conceptualization, methodology, and interpretation of the findings; AMP collected and analyzed the data, drafted the manuscript, and prepared figures; LHT and GH provided feedback throughout data analyses and revision of the manuscript and figures.
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Communicated by Bill J Yates.
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Payne, A.M., Ting, L.H. & Hajcak, G. The balance N1 and the ERN correlate in amplitude across individuals in small samples of younger and older adults. Exp Brain Res 241, 2419–2431 (2023). https://doi.org/10.1007/s00221-023-06692-9
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DOI: https://doi.org/10.1007/s00221-023-06692-9