Investigating mechanisms of cognitive control training: neural signatures of PASAT performance in depressed patients

Anja Sommer, Andreas J Fallgatter, Christian Plewnia, Anja Sommer, Andreas J Fallgatter, Christian Plewnia

Abstract

Major depression disorder (MDD) is characterized by cognitive control (CC) dysfunctions associated with increased attention toward negative information. The paced auditory serial addition task (PASAT) has been used as a targeted training of CC and studies show promising effects on depressive symptoms. However, neural mechanisms underlying its efficacy are still unclear. Based on previous findings of feedback-locked event-related potentials in healthy subjects, we investigated neural signatures during PASAT performance in 46 depressed patients. We found significantly larger amplitudes after negative than positive feedback for the P300 and late positive potential (LPP). However, this difference was not significant for the feedback-related negativity (FRN). Moreover, no associations of valence-specific ERPs and PASAT performance nor depressive symptoms were found. This indicates that depressed patients seem unable to use neural activation in late feedback processing stages (P300, LPP) to adapt accordingly. Moreover, lack of valence-specific neural reaction in early feedback processing stages (FRN) might point toward emotional indifference in depressed patients.Trial registration number: NCT03518749 Date of registration: May 8, 2018.

Keywords: Cognitive control; Cognitive control training; Event-related potentials; Major depressive disorder; PASAT; dlPFC.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

© 2021. The Author(s).

Figures

Fig. 1
Fig. 1
Feedback-related negativity. Grand average waveform at Fz and scalp map displaying the mean voltage distribution (200–300 ms post-feedback) of the feedback-related negativity, separately for negative and positive feedbacks
Fig. 2
Fig. 2
P300. Grand average waveform averaged across Cz, CPz, Pz, and scalp map displaying the mean voltage distribution (300–400 ms post-feedback) separately for negative and positive feedbacks of the P300
Fig. 3
Fig. 3
Late positive potential. Grand average waveform averaged across Cz, CPz, Pz, CP1, CP2, and scalp map displaying the mean voltage distribution (300–400 ms post-feedback) separately for negative and positive feedbacks of the LPP

References

    1. Baert S, De Raedt R, Koster EHW. Depression-related attentional bias: the influence of symptom severity and symptom specificity. Cogn Emot. 2010;24:1044–1052. doi: 10.1080/02699930903043461.
    1. Bellebaum C, Daum I. Learning-related changes in reward expectancy are reflected in the feedback-related negativity. Eur J Neurosci. 2008;27:1823–1835. doi: 10.1111/j.1460-9568.2008.06138.x.
    1. Blackburn IM, Roxborough HM, Muir WJ, et al. Perceptual and physiological dysfunction in depression. Psychol Med. 1990;20:95–103. doi: 10.1017/S003329170001326X.
    1. Cacioppo JT, Crites SL, Gardner WL. Attitudes to the right: Evaluative processing is associated with lateralized late positive event-related brain potentials. Personal Soc Psychol Bull. 1996;22:1205–1219. doi: 10.1177/01461672962212002.
    1. Cavanagh JF, Bismark AJ, Frank MJ, et al. Larger error signals in major depression are associated with better avoidance learning. Front Psychol. 2011;2:1–6. doi: 10.3389/fpsyg.2011.00331.
    1. Cuthbert BN, Schupp HT, Bradley MM, et al. Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol Psychol. 2000;52:95–111. doi: 10.1016/S0301-0511(99)00044-7.
    1. Delorme A, Makeig S. EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004;134:9–21. doi: 10.1016/j.jneumeth.2003.10.009.
    1. Diner BC, Holcomb PJ, Dykman RA. P300 in major depressive disorder. Psychiatry Res. 1985;15:175–184. doi: 10.1016/0165-1781(85)90074-5.
    1. Fabiani M, Gratton G, Karis D, et al. Definition identification, and reliability of measurement of the P300 component of the eventrelated brain potential. Adv Psychophysiol. 1987;2:1–78.
    1. Fales CL, Barch DM, Rundle MM, et al. Altered emotional interference processing in affective and cognitive-control brain circuitry in major depression. Biol Psychiatry. 2008;63:377–384. doi: 10.1016/j.biopsych.2007.06.012.
    1. Fischer BA. A Review of american psychiatry through its diagnoses: the history and development of the diagnostic and statistical manual of mental disorders. J Nerv Ment Dis. 2012;200:1022–1030. doi: 10.1097/NMD.0b013e318275cf19.
    1. Foti D, Hajcak G. Depression and reduced sensitivity to non-rewards versus rewards: evidence from event-related potentials. Biol Psychol. 2009;81:1–8. doi: 10.1016/j.biopsycho.2008.12.004.
    1. Foti D, Olvet DM, Klein DN, et al. Reduced electrocortical response to threatening faces in major depressive disorder. Depress Anxiety. 2010;27:813–820. doi: 10.1002/da.20712.
    1. Gangadhar BN, Ancy J, Janakiranaiah N, et al. P300 amplitude in non-bipolar, melancholic depression. J Affect Disord. 1993;28:57–60. doi: 10.1016/0165-0327(93)90077-W.
    1. Gehring WJ, Willoughby AR. The medial frontal cortex and the rapid processing of monetary gains and losses. Science (80-) 2002;295:2279–2282. doi: 10.1126/science.106689380-.
    1. Gotlib IH, Joormann J. Cognition and depression: current status and future directions. Annu Rev Clin Psychol. 2010;6:285–312. doi: 10.1146/annurev.clinpsy.121208.131305.
    1. Gronwall D. Paced auditory serial-addition task: a measure of recovery from concussion. Percept Mot Skills. 1977;44:367–373. doi: 10.2466/pms.1977.44.2.367.
    1. Hajcak G, Moser JS, Holroyd CB, et al. The feedback-related negativity reflects the binary evaluation of good versus bad outcomes. Biol Psychol. 2006;71:148–154. doi: 10.1016/j.biopsycho.2005.04.001.
    1. Hajcak G, Dunning JP, Foti D. Motivated and controlled attention to emotion: time-course of the late positive potential. Clin Neurophysiol. 2009;120:505–510. doi: 10.1016/j.clinph.2008.11.028.
    1. Holdwick DJJ, Wingenfeld SA. The subjective experience of PASAT testing. Does the PASAT induce negative mood? Arch Clin Neuropsychol off J Natl Acad Neuropsychol. 1999;14:273–284. doi: 10.1093/arclin/14.3.273.
    1. Hoorelbeke K, Koster EHW, Vanderhasselt M-A, et al. The influence of cognitive control training on stress reactivity and rumination in response to a lab stressor and naturalistic stress. Behav Res Ther. 2015;69:1–10. doi: 10.1016/j.brat.2015.03.010.
    1. Ito TA, Larsen JT, Smith NK, et al. Negative information weighs more heavily on the brain: the negativity bias in evaluative categorizations. J Pers Soc Psychol. 1998;75:887–900. doi: 10.1037/0022-3514.75.4.887.
    1. Johnson RJ. On the neural generators of the P300 component of the event-related potential. Psychophysiology. 1993;30:90–97. doi: 10.1111/j.1469-8986.1993.tb03208.x.
    1. Keren H, O’Callaghan G, Vidal-Ribas P, et al. Reward processing in depression: a conceptual and meta-analytic review across fMRI and EEG studies. Am J Psychiatry. 2018;175:1111–1120. doi: 10.1176/appi.ajp.2018.17101124.
    1. Klawohn J, Burani K, Bruchnak A, et al. Reduced neural response to reward and pleasant pictures independently relate to depression. Psychol Med. 2020 doi: 10.1017/S0033291719003659.
    1. Koster EHW, Hoorelbeke K, Onraedt T, et al. Cognitive control interventions for depression: a systematic review of findings from training studies. Clin Psychol Rev. 2017;53:79–92. doi: 10.1016/j.cpr.2017.02.002.
    1. Krohne HW, Egloff B, Kohlmann C-W, et al. Untersuchungen mit einer deutschen version der “Positive and Negative Affect Schedule” (PANAS). [investigations with a german version of the positive and negative affect schedule (PANAS).] Diagnostica. 1996;42:139–156.
    1. Lass ANS, Rokke PD, Winer ES. Evaluating cognitive control training on symptoms of depression over time: three potential mechanisms. J Affect Disord Rep. 2021;4:100127. doi: 10.1016/j.jadr.2021.100127.
    1. Lazeron RH, Rombouts SAR, de Sonneville L, et al. A paced visual serial addition test for fMRI. J Neurol Sci. 2003;213:29–34. doi: 10.1016/S0022-510X(03)00144-8.
    1. LeMoult J, Gotlib IH. Depression: a cognitive perspective. Clin Psychol Rev. 2019;69:51–66. doi: 10.1016/j.cpr.2018.06.008.
    1. Liu W, Wang L, Shang H, et al. The influence of anhedonia on feedback negativity in major depressive disorder. Neuropsychologia. 2014;53:213–220. doi: 10.1016/j.neuropsychologia.2013.11.023.
    1. Lopez-Calderon J, Luck SJ. ERPLAB: an open-source toolbox for the analysis of event-related potentials. Front Hum Neurosci. 2014;8:213. doi: 10.3389/fnhum.2014.00213.
    1. Luu P, Tucker DM, Derryberry D, et al. Electrophysiological responses to errors and feedback in the process of action regulation. Psychol Sci. 2003;14:47–53. doi: 10.1111/1467-9280.01417.
    1. Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134:382–389. doi: 10.1192/bjp.134.4.382.
    1. Moser JS, Hajcak G, Bukay E, et al. Intentional modulation of emotional responding to unpleasant pictures: an ERP study. Psychophysiology. 2006;43:292–296. doi: 10.1111/j.1469-8986.2006.00402.x.
    1. Mueller EM, Pechtel P, Cohen AL, et al. Potentiated processing of negative feedback in depression is attenuated by anhedonia. Depress Anxiety. 2015;32:296–305. doi: 10.1002/da.22338.
    1. Nan C, Wang G, Wang H, et al. The P300 component decreases in a bimodal oddball task in individuals with depression: an event-related potentials study. Clin Neurophysiol. 2018;129:2525–2533. doi: 10.1016/j.clinph.2018.09.012.
    1. Peirce JW. PsychoPy—psychophysics software in Python. J Neurosci Methods. 2007;162:8–13. doi: 10.1016/j.jneumeth.2006.11.017.
    1. Peirce JW. Generating stimuli for neuroscience using PsychoPy. Front Neuroinform. 2008;2:10. doi: 10.3389/neuro.11.010.2008.
    1. Plewnia C, Schroeder PA, Kunze R, et al. Keep calm and carry on: improved frustration tolerance and processing speed by transcranial direct current stimulation (tDCS) PLoS ONE. 2015;10:e0122578. doi: 10.1371/journal.pone.0122578.
    1. Polich J. P300 in clinical applications: meaning, method, and measurement. Am J EEG Technol. 1991;31:201–231. doi: 10.1080/00029238.1991.11080373.
    1. Polich J. Neuropsychology of P300. In: Luck SJ, Kappenman ES, editors. The Oxford handbook of event related potential component. New York: Oxford University Press; 2012. pp. 159–188.
    1. Polich J, Kok A. Cognitive and biological determinants of P300: an integrative review. Biol Psychol. 1995;41:103–146. doi: 10.1016/0301-0511(95)05130-9.
    1. Proudfit GH. The reward positivity: from basic research on reward to a biomarker for depression. Psychophysiology. 2015;52:449–459. doi: 10.1111/psyp.12370.
    1. Proudfit GH, Bress JN, Foti D, et al. Depression and event-related potentials: emotional disengagement and reward insensitivity. Curr Opin Psychol. 2015;4:110–113. doi: 10.1016/j.copsyc.2014.12.018.
    1. Ridderinkhof KR, Ullsperger M, Crone EA, et al. The role of the medial frontal cortex in cognitive control. Science (80-) 2004;306:443–447. doi: 10.1126/science.1100301.
    1. Santesso DL, Steele KT, Bogdan R, et al. Enhanced negative feedback responses in remitted depression. NeuroReport. 2008;19:1045–1048. doi: 10.1097/WNR.0b013e3283036e73.
    1. Siegle GJ, Ghinassi F, Thase ME. Neurobehavioral therapies in the 21st century: summary of an emerging field and an extended example of cognitive control training for depression. Cognit Ther Res. 2007;31:235–262. doi: 10.1007/s10608-006-9118-6.
    1. Siegle GJ, Thompson W, Carter CS, et al. Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol Psychiatry. 2007;61:198–209. doi: 10.1016/j.biopsych.2006.05.048.
    1. Siegle GJ, Price RB, Jones NP, et al. You gotta work at it: pupillary indices of task focus are prognostic for response to a neurocognitive intervention for rumination in depression. Clin Psychol Sci. 2014;2:455–471. doi: 10.1177/2167702614536160.
    1. Sommer A, Plewnia C. Depression treatment by tDCS-enhanced cognitive control training: a test of two stimulation intensities. Brain Stimul. 2021 doi: 10.1016/j.brs.2021.06.004.
    1. Sommer A, Ecker L, Plewnia C. Neural signatures of performance feedback in the paced auditory serial addition task (PASAT): an ERP study. Front Hum Neurosci. 2021;15:71.
    1. Sutton S, Braren M, Zubin J, et al. Evoked-potential correlates of stimulus uncertainty. Science (80-) 1965;150:1187–1188. doi: 10.1126/science.150.3700.1187.
    1. Tucker DM, Luu P, Frishkoff G, et al. Frontolimbic response to negative feedback in clinical depression. J Abnorm Psychol. 2003;112:667–678. doi: 10.1037/0021-843X.112.4.667.
    1. Van den Bergh N, Hoorelbeke K, De Raedt R, et al. Remediation of depression-related cognitive impairment: cognitive control training as treatment augmentation. Expert Rev Neurother. 2018;18:907–913. doi: 10.1080/14737175.2018.1537783.
    1. Weinberg A, Hajcak G. Beyond good and evil: the time-course of neural activity elicited by specific picture content. Emotion. 2010;10:767–782. doi: 10.1037/a0020242.
    1. Weismüller B, Bellebaum C. Expectancy affects the feedback-related negativity (FRN) for delayed feedback in probabilistic learning. Psychophysiology. 2016;53:1739–1750. doi: 10.1111/psyp.12738.
    1. Weiß M, Rodrigues J, Boschet JM, et al. How depressive symptoms and fear of negative evaluation affect feedback evaluation in social decision-making. J Affect Disord Rep. 2020;1:100004. doi: 10.1016/j.jadr.2020.100004.

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren