Neurocognitive mechanisms behind emotional attention: Inverse effects of anodal tDCS over the left and right DLPFC on gaze disengagement from emotional faces

  • Alvaro Sanchez-LopezEmail author
  • Marie-Anne Vanderhasselt
  • Jens Allaert
  • Chris Baeken
  • Rudi De Raedt



Attention to relevant emotional information in the environment is an important process related to vulnerability and resilience for mood and anxiety disorders. In the present study, the effects of left and right dorsolateral prefrontal cortex (i.e., DLPFC) stimulation on attentional mechanisms of emotional processing were tested and contrasted.


A sample of 54 healthy participants received 20 min of active and sham anodal transcranial direct current stimulation (i.e., tDCS) either of the left (n = 27) or of the right DLPFC (n = 27) on two separate days. The anode electrode was placed over the left or the right DLPFC, the cathode over the corresponding contra lateral supraorbital area. After each neurostimulation session, participants completed an eye-tracking task assessing direct processes of attentional engagement towards and attentional disengagement away from emotional faces (happy, disgusted, and sad expressions).


Compared to sham, active tDCS over the left DLPFC led to faster gaze disengagement, whereas active tDCS over the right DLPFC led to slower gaze disengagement from emotional faces. Between-group comparisons showed that such inverse change patterns were significantly different and generalized for all types of emotion.


Our findings support a lateralized role of left and right DLPFC activity in enhancing/worsening the top-down regulation of emotional attention processing. These results support the rationale of new therapies for affective disorders aimed to increase the activation of the left over the right DLPFC in combination with attentional control training, and identify specific target attention mechanisms to be trained.


Selective attention, Attentional control, Emotion, DLPFC, Neurostimulation 



This research was supported by a grant FWO (ref. 117438) awarded to Alvaro Sanchez, a grant BOF16/GOA/017 awarded to Rudi De Raedt, and the Ghent University Multidisciplinary Research Partnership “The integrative neuroscience of behavioral control.”


  1. Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Manual for the Beck Depression Inventory - II. San Antonio, TX: Psychological Corporation.Google Scholar
  2. Chen, N. T. M., Basanovic, J., Notebaert, L., MacLeod, C., & Clarke, P. J. F. (2017). Attentional bias mediates the effect of neurostimulation on emotional vulnerability. Journal of Psychiatric Research, 93, 12–19. CrossRefPubMedGoogle Scholar
  3. Clarke, P. J. F., Browning, M., Hammond, G., Notebaert, L., & MacLeod, C. (2014). The Causal Role of the Dorsolateral Prefrontal Cortex in the Modification of Attentional Bias: Evidence from Transcranial Direct Current Stimulation. Biological Psychiatry, 76(12), 946–952. CrossRefPubMedGoogle Scholar
  4. Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 215–229. CrossRefGoogle Scholar
  5. De Raedt, R., & Koster, E. H. W. (2010). Understanding vulnerability for depression from a cognitive neuroscience perspective: A reappraisal of attentional factors and a new conceptual framework. Cognitive, Affective & Behavioral Neuroscience, 10(1), 50–70. CrossRefGoogle Scholar
  6. De Raedt, R., Leyman, L., Baeken, C., Van Schuerbeek, P., Luypaert, R., Vanderhasselt, M. A., & Dannlowski, U. (2010). Neurocognitive effects of HF-rTMS over the dorsolateral prefrontal cortex on the attentional processing of emotional information in healthy women: An event-related fMRI study. Biol Psychol, 85(3), 487–495. CrossRefPubMedGoogle Scholar
  7. De Raedt, R., Vanderhasselt, M.-A., & Baeken, C. (2015). Neurostimulation as an intervention for treatment resistant depression: From research on mechanisms towards targeted neurocognitive strategies. Clinical Psychology Review, 41, 61–69. CrossRefPubMedGoogle Scholar
  8. Dinn, W., Göral, F., Adigüzel, S., Karamürsel, S., Fregni, F., & Aycicegi-Dinn, A. (2017) Effectiveness of tDCS blinding protocol in a sham-controlled study. Brain Stimulation, 10, 401.
  9. Disner, S. G. S., Beevers, C. G. C., Haigh, EA. & Beck, A. T. (2011). Neural mechanisms of the cognitive model of depression. Nature Reviews. Neuroscience, 12(8), 467–477.
  10. Gross, J. J., Sheppes, G., & Urry, H. L. (2011). Cognition and Emotion Lecture at the 2010 SPSP Emotion Preconference. Cognition & Emotion, 25(5), 765–781. CrossRefGoogle Scholar
  11. Heeren, A., Baeken, C., Vanderhasselt, M.-A., Philippot, P., & de Raedt, R. (2015). Impact of Anodal and Cathodal Transcranial Direct Current Stimulation over the Left Dorsolateral Prefrontal Cortex during Attention Bias Modification: An Eye-Tracking Study. PloS One, 10(4), e0124182. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Heeren, A., Billieux, J., Philippot, P., De Raedt, R., Baeken, C., de Timary, P., … Vanderhasselt, M.-A. (2016). Impact of transcranial direct current stimulation on attentional bias for threat: a proof-of-concept study among individuals with social anxiety disorder. Social Cognitive and Affective Neuroscience, (September 2016).
  13. Heinze, K., Ruh, N., Nitschke, K., Reis, J., Fritsch, B., Unterrainer, J. M., … Kaller, C. P. (2014). Transcranial direct current stimulation over left and right DLPFC: Lateralized effects on planning performance and related eye movements. Biological Psychology, 102(January), 130–140. CrossRefPubMedGoogle Scholar
  14. Ironside, M. M., O’Shea, J., Cowen, P.J., & CJ Harmer. (2015). Frontal cortex stimulation reduces vigilance to threat: implications for the treatsment of depression and anxiety. Biological Psychiatry, (4), 1–8.
  15. Kalu, U. G., Sexton, C. E., Loo, C. K., & Ebmeier, K. P. (2012). Transcranial direct current stimulation in the treatment of major depression: A meta-analysis. Psychological Medicine, 42(9), 1791–1800. CrossRefPubMedGoogle Scholar
  16. Keeser, D., Meindl, T., Bor, J., Palm, U., Pogarell, O., Mulert, C., … Padberg, F. (2011). Prefrontal Transcranial Direct Current Stimulation Changes Connectivity of Resting-State Networks during fMRI. Journal of Neuroscience, 31(43), 15284–15293. CrossRefPubMedGoogle Scholar
  17. Langner, O., Dotsch, R., Bijlstra, G., Wigboldus, D. H. J., Hawk, S. T., & van Knippenberg, A. (2010). Presentation and validation of the Radboud Faces Database. Cognition & Emotion, 24(8), 1377–1388. CrossRefGoogle Scholar
  18. Leyman, L., De Raedt, R., Schacht, R., & Koster, E. H. W. (2007). Attentional biases for angry faces in unipolar depression. Psychological Medicine, 37(3), 393. CrossRefPubMedGoogle Scholar
  19. Leyman, L., Raedt, R. De, Vanderhasselt, M. A., & Baeken, C. (2011). Effects of repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex on the attentional processing of emotional information in major depression: A …. Psychiatry Research. Retrieved from
  20. Loo, C. K., Alonzo, A., Martin, D., Mitchell, P. B., Galvez, V., & Sachdev, P. (2012). Transcranial direct current stimulation for depression: 3-Week, randomised, sham-controlled trial. British Journal of Psychiatry, 200(1), 52–59. CrossRefPubMedGoogle Scholar
  21. MacDonald, A. W., Cohen, J. D., Stenger, V. A., & Carter, C. S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288(5472), 1835–1838. Retrieved from CrossRefPubMedGoogle Scholar
  22. McCormack, H. M., Horne, D. J. L., & Sheather, S. (1988). Clinical application of visual analogue scales: A critical review. Psychological Medicine, 18, 1007–1019.CrossRefPubMedGoogle Scholar
  23. Nitsche, M. A., Boggio, P. S., Fregni, F., & Pascual-Leone, A. (2009). Treatment of depression with transcranial direct current stimulation (tDCS): A Review. Experimental Neurology, 219(1), 14–19. CrossRefPubMedGoogle Scholar
  24. Nitsche, M. A., Cohen, L. G., Wassermann, E. M., Priori, A., Lang, N., Antal, A., … Pascual-Leone, A. (2008). Transcranial direct current stimulation: State of the art 2008. Brain Stimulation.
  25. Ochsner, K. N., & Gross, J. J. (2005). The cognitive control of emotion. Trends in Cognitive Sciences, 9, 242-249.
  26. Opitz, A., Paulus, W., Will, S., Antunes, A., & Thielscher, A. (2015). Determinants of the electric field during transcranial direct current stimulation. NeuroImage, 109, 140–150. CrossRefPubMedGoogle Scholar
  27. Overbeek, T., Schruers, K., & Griez, E. (1999). Mini International Neuropsychiatric Interview. Maastricht: University of Maastricht.Google Scholar
  28. Posner, M. I., & Cohen, Y. (1984). Components of visual orienting. Attention and Performance: Control of Language Processes, 531–556.
  29. Remue, J., Baeken, C., & De Raedt, R. (2016). Does a single neurostimulation session really affect mood in healthy individuals? A systematic review. Neuropsychologia.
  30. Sanchez, A., Romero, N., & De Raedt, R. (2017). Depression-related difficulties disengaging from negative faces are associated with sustained attention to negative feedback during social evaluation and predict stress recovery. PLoS ONE, 12(3), 1–24. CrossRefGoogle Scholar
  31. Sanchez, A., Vanderhasselt, M.-A., Baeken, C., & De Raedt, R. (2016). Effects of tDCS over the right DLPFC on attentional disengagement from positive and negative faces: An eye-tracking study. Cognitive, Affective, & Behavioral Neuroscience, 16(6), 1027–1038. CrossRefGoogle Scholar
  32. Sanchez, A., Vazquez, C., Marker, C., LeMoult, J., & Joormann, J. (2013). Attentional disengagement predicts stress recovery in depression: An eye-tracking study. Journal of Abnormal Psychology, 122(2), 303–313. CrossRefPubMedGoogle Scholar
  33. Schofield, C. a., Johnson, A. L., Inhoff, A. W., & Coles, M. E. (2012). Social anxiety and difficulty disengaging threat: Evidence from eye-tracking. Cognition & Emotion, 26(2), 300–311. CrossRefGoogle Scholar
  34. Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Janavs, J., Weiller, E., Keskiner, A., … Dunbar, G. C. (1997). The validity of the Mini International Neuropsychiatric Interview (MINI) according to the SCID-P and its reliability. European Psychiatry, 12(5), 232–241. CrossRefGoogle Scholar
  35. Spielberger, C. D., Gorsuch, R. L., Lushene, R., Vagg, P. R., & Jacobs, G. A. (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
  36. Stagg, C. J., Best, J. G., Stephenson, M. C., O’Shea, J., Wylezinska, M., Kincses, Z. T., … Johansen-Berg, H. (2009). Polarity-Sensitive Modulation of Cortical Neurotransmitters by Transcranial Stimulation. Journal of Neuroscience, 29(16), 5202–5206. CrossRefPubMedGoogle Scholar
  37. Van der Does, A. J. W. (2002). Handleiding bij de Nederlandse versie van de Beck Depression Inventory - second edition (BDI-II-NL). [The Dutch version of the Beck Depresion Inventory-II]. Lisse, The Netherlands: Swets & Zeitlinger.Google Scholar
  38. van der Ploeg, H. M., Defares, P. B., & Spielberger, C. D. (1980). Handleiding bij de Zelf-Beoordelings Vragenlijst, ZBV. Een Nederlandstalige bewerking van de Spielberger State-Trait Anxiety Inventory, STAT-DY. Lisse: Swets en Zeitlinger.Google Scholar
  39. Vanderhasselt, M. A., De Raedt, R., Baeken, C., Leyman, L., & D’haenen, H. (2006). The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance. Experimental Brain Research, 169(2), 279–282. CrossRefPubMedGoogle Scholar
  40. Vanderhasselt, M. A., De Raedt, R., Brunoni, A. R., Campanhã, C., Baeken, C., Remue, J., & Boggio, P. S. (2013). tDCS over the Left Prefrontal Cortex Enhances Cognitive Control for Positive Affective Stimuli. PLoS ONE, 8(5).

Copyright information

© Psychonomic Society, Inc. 2018

Authors and Affiliations

  1. 1.Department of Experimental Clinical and Health PsychologyGhent UniversityGhentBelgium
  2. 2.Complutense University of MadridMadridSpain

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