Brain Structure and Function

, Volume 219, Issue 3, pp 995–1008 | Cite as

Probing emotional influences on cognitive control: an ALE meta-analysis of cognition emotion interactions

  • Sofie Cromheeke
  • Sven C. MuellerEmail author
Original Article


Increasing research documents an integration of cognitive control and affective processes. Despite a surge of interest in investigating the exact nature of this integration, no consensus has been reached on the precise neuroanatomical network involved. Using the activation likelihood estimation meta-analysis method, we examined 43 functional magnetic resonance imaging (fMRI) studies (total number of foci = 332; total number of participants, N = 820) from the literature that have reported significant interactions between emotion and cognitive control. Meta-analytic results revealed that concurrent emotion (relative to emotionally neutral trials) consistently increased neural activation during high relative to low cognitive control conditions across studies and paradigms. Specifically, these activations emerged in regions commonly implicated in cognitive control, such as the lateral prefrontal cortex (inferior frontal junction, inferior frontal gyrus), the medial prefrontal cortex, and the basal ganglia. In addition, some areas emerged during the interaction contrast that were not present during one of the main effects and included the subgenual anterior cingulate cortex and the precuneus. These data provide new evidence for a network of cognition emotion interaction within a cognitive control setting. The findings are discussed within current theories of cognitive and attentional control.


Meta-analysis fMRI Executive function Emotion Affective 



We acknowledge the support of Ghent University (Multidisciplinary Research Partnership “The integrative neuroscience of behavioural control”). We would also like to thank the two anonymous reviewers and Marcel Brass for valuable suggestions on an earlier version of this manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

429_2013_549_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 23 kb)
429_2013_549_MOESM2_ESM.docx (20 kb)
Supplementary material 2 (DOCX 20 kb)


  1. Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8(4):170–177PubMedCrossRefGoogle Scholar
  2. Ashby FG, Isen AM, Turken AU (1999) A neuropsychological theory of positive affect and its influence on cognition. Psychol Rev 106(3):529–550PubMedCrossRefGoogle Scholar
  3. Banich MT, Mackiewicz KL, Depue BE, Whitmer AJ, Miller GA, Heller W (2009) Cognitive control mechanisms, emotion and memory: a neural perspective with implications for psychopathology. Neurosci Biobehav Rev 33(5):613–630PubMedCentralPubMedCrossRefGoogle Scholar
  4. Blair KS, Smith BW, Mitchell DG, Morton J, Vythilingam M, Pessoa L, Fridberg D, Zametkin A, Sturman D, Nelson EE, Drevets WC, Pine DS, Martin A, Blair RJ (2007) Modulation of emotion by cognition and cognition by emotion. NeuroImage 35(1):430–440PubMedCentralPubMedCrossRefGoogle Scholar
  5. Botvinick M, Nystrom LE, Fissell K, Carter CS, Cohen JD (1999) Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402(6758):179–181PubMedCrossRefGoogle Scholar
  6. Brass M, Derrfuss J, Forstmann B, von Cramon DY (2005) The role of the inferior frontal junction area in cognitive control. Trends Cogn Sci 9(7):314–316PubMedCrossRefGoogle Scholar
  7. Brooks SJ, Savov V, Allzen E, Benedict C, Fredriksson R, Schioth HB (2012) Exposure to subliminal arousing stimuli induces robust activation in the amygdala, hippocampus, anterior cingulate, insular cortex and primary visual cortex: a systematic meta-analysis of fMRI studies. NeuroImage 59(3):2962–2973PubMedCrossRefGoogle Scholar
  8. Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4(6):215–222PubMedCrossRefGoogle Scholar
  9. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129(Pt 3):564–583PubMedCrossRefGoogle Scholar
  10. Chechko N, Wehrle R, Erhardt A, Holsboer F, Czisch M, Samann PG (2009) Unstable prefrontal response to emotional conflict and activation of lower limbic structures and brainstem in remitted panic disorder. PLoS ONE 4(5):e5537PubMedCentralPubMedCrossRefGoogle Scholar
  11. Choi HJ, Zilles K, Mohlberg H, Schleicher A, Fink GR, Armstrong E, Amunts K (2006) Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus. J Comp Neurol 495(1):53–69PubMedCentralPubMedCrossRefGoogle Scholar
  12. Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215PubMedCrossRefGoogle Scholar
  13. Damasio H (2005) Human Brain anatomy in computerized images. Oxford University Press, OxfordCrossRefGoogle Scholar
  14. Deckersbach T, Rauch SL, Buhlmann U, Ostacher MJ, Beucke JC, Nierenberg AA, Sachs G, Dougherty DD (2008) An fMRI investigation of working memory and sadness in females with bipolar disorder: a brief report. Bipolar Disord 10(8):928–942PubMedCrossRefGoogle Scholar
  15. Derrfuss J, Brass M, Neumann J, von Cramon YD (2005) Involvement of the inferior frontal junction in cognitive control: meta-analyses of switching and Stroop studies. Human Brain Mapp 25:22–34CrossRefGoogle Scholar
  16. Diekhof EK, Geier K, Falkai P, Gruber O (2011) Fear is only as deep as the mind allows: a coordinate-based meta-analysis of neuroimaging studies on the regulation of negative affect. NeuroImage 58(1):275–285PubMedCrossRefGoogle Scholar
  17. Dolcos F, McCarthy G (2006) Brain systems mediating cognitive interference by emotional distraction. J Neurosci 26(7):2072–2079PubMedCrossRefGoogle Scholar
  18. Drevets WC, Savitz J (2008) The subgenual anterior cingulate cortex in mood disorders. CNS Spectr 13(8):663–681PubMedCentralPubMedGoogle Scholar
  19. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30(9):2907–2926PubMedCentralPubMedCrossRefGoogle Scholar
  20. Freedman LJ, Insel TR, Smith Y (2000) Subcortical projections of area 25 (subgenual cortex) of the macaque monkey. J Comp Neurol 421(2):172–188PubMedCrossRefGoogle Scholar
  21. Fruhholz S, Fehr T, Herrmann M (2009) Interference control during recognition of facial affect enhances the processing of expression specific properties—an event-related fMRI study. Brain Res 1269:143–157PubMedCrossRefGoogle Scholar
  22. Goldstein M, Brendel G, Tuescher O, Pan H, Epstein J, Beutel M, Yang Y, Thomas K, Levy K, Silverman M, Clarkin J, Posner M, Kernberg O, Stern E, Silbersweig D (2007) Neural substrates of the interaction of emotional stimulus processing and motor inhibitory control: an emotional linguistic go/no-go fMRI study. NeuroImage 36(3):1026–1040PubMedCrossRefGoogle Scholar
  23. Gray JR (2001) Emotional modulation of cognitive control: approach-withdrawal states double-dissociate spatial from verbal two-back task performance. J Exp Psychol Gen 130(3):436–452PubMedCrossRefGoogle Scholar
  24. Gray JR, Braver TS, Raichle ME (2002) Integration of emotion and cognition in the lateral prefrontal cortex. Proc Natl Acad Sci USA 99(6):4115–4120PubMedCentralPubMedCrossRefGoogle Scholar
  25. Habel U, Koch K, Pauly K, Kellermann T, Reske M, Backes V, Seiferth NY, Stocker T, Kircher T, Amunts K, Jon Shah N, Schneider F (2007) The influence of olfactory-induced negative emotion on verbal working memory: individual differences in neurobehavioral findings. Brain Res 1152:158–170PubMedCrossRefGoogle Scholar
  26. Hart SJ, Green SR, Casp M, Belger A (2010) Emotional priming effects during Stroop task performance. NeuroImage 49(3):2662–2670PubMedCentralPubMedCrossRefGoogle Scholar
  27. Kanske P, Kotz SA (2011) Emotion speeds up conflict resolution: a new role for the ventral anterior cingulate cortex? Cereb Cortex 21(4):911–919PubMedCrossRefGoogle Scholar
  28. Laird AR, Robinson JL, McMillan KM, Tordesillas-Gutierrez D, Moran ST, Gonzales SM, Ray KL, Franklin C, Glahn DC, Fox PT, Lancaster JL (2010) Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: validation of the Lancaster transform. NeuroImage 51(2):677–683PubMedCentralPubMedCrossRefGoogle Scholar
  29. Lancaster JL, Tordesillas-Gutierrez D, Martinez M, Salinas F, Evans A, Zilles K, Mazziotta JC, Fox PT (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28(11):1194–1205PubMedCrossRefGoogle Scholar
  30. Levens SM, Phelps EA (2010) Insula and orbital frontal cortex activity underlying emotion interference resolution in working memory. J Cogn Neurosci 22(12):2790–2803PubMedCrossRefGoogle Scholar
  31. Liu X, Banich MT, Jacobson BL, Tanabe JL (2004) Common and distinct neural substrates of attentional control in an integrated Simon and spatial Stroop task as assessed by event-related fMRI. NeuroImage 22(3):1097–1106PubMedCrossRefGoogle Scholar
  32. Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, Biswal BB, Villringer A, Castellanos FX, Milham MP, Petrides M (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106(47):20069–20074PubMedCentralPubMedCrossRefGoogle Scholar
  33. Mather M, Mitchell KJ, Raye CL, Novak DL, Greene EJ, Johnson MK (2006) Emotional arousal can impair feature binding in working memory. J Cogn Neurosci 18(4):614–625PubMedCrossRefGoogle Scholar
  34. Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214(5–6):655–667PubMedCentralPubMedCrossRefGoogle Scholar
  35. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202PubMedCrossRefGoogle Scholar
  36. Mueller SC (2011) The influence of emotion on cognitive control: relevance for development and adolescent psychopathology. Front Psychol 2:327. doi: 10.3389/fpsyg.2011.00327
  37. Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25(1):46–59PubMedCrossRefGoogle Scholar
  38. Padmala S, Pessoa L (2010) Interactions between cognition and motivation during response inhibition. Neuropsychologia 48(2):558–565PubMedCentralPubMedCrossRefGoogle Scholar
  39. Pereira MG, de Oliveira L, Erthal FS, Joffily M, Mocaiber IF, Volchan E, Pessoa L (2010) Emotion affects action: midcingulate cortex as a pivotal node of interaction between negative emotion and motor signals. Cogn Affect Behav Neurosci 10(1):94–106PubMedCentralPubMedCrossRefGoogle Scholar
  40. Pessoa L (2008) On the relationship between emotion and cognition. Nat Rev Neurosci 9(2):148–158PubMedCrossRefGoogle Scholar
  41. Price JL, Drevets WC (2010) Neurocircuitry of mood disorders. Neuropsychopharmacology 35(1):192–216PubMedCentralPubMedCrossRefGoogle Scholar
  42. Roseman IJ (2008) Motivations and emotivations: approach, avoidance, and other tendencies in motivated and emotional behavior. Handbook of approach and avoidance motivation. Psychology Press, A. J. Elliot, New York, pp 343–366Google Scholar
  43. Schulz KP, Clerkin SM, Halperin JM, Newcorn JH, Tang CY, Fan J (2009) Dissociable neural effects of stimulus valence and preceding context during the inhibition of responses to emotional faces. Hum Brain Mapp 30(9):2821–2833PubMedCentralPubMedCrossRefGoogle Scholar
  44. Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ (2011) The integration of negative effect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 12(3):154–167PubMedCentralPubMedCrossRefGoogle Scholar
  45. Sutton SK, Davidson RJ (1997) Prefrontal brain asymmetry: a biological substrate of the behavioral approach and inhibition systems. Psychol Sci 8(3):204–210CrossRefGoogle Scholar
  46. Swick D, Ashley V, Turken U (2011) Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. NeuroImage 56(3):1655–1665PubMedCrossRefGoogle Scholar
  47. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, StuttgartGoogle Scholar
  48. Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA (2002) Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. NeuroImage 16(3 Pt 1):765–780PubMedCrossRefGoogle Scholar
  49. Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P (2012) Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum Brain Mapp 33(1):1–13PubMedCrossRefGoogle Scholar
  50. Uddin LQ, Supekar K, Amin H, Rykhlevskaia E, Nguyen DA, Greicius MD, Menon V (2010) Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cereb Cortex 20(11):2636–2646PubMedCentralPubMedCrossRefGoogle Scholar
  51. van der Laan LN, de Ridder DT, Viergever MA, Smeets PA (2011) The first taste is always with the eyes: a meta-analysis on the neural correlates of processing visual food cues. NeuroImage 55(1):296–303PubMedCrossRefGoogle Scholar
  52. Van Dillen LF, Heslenfeld DJ, Koole SL (2009) Tuning down the emotional brain: an fMRI study of the effects of cognitive load on the processing of affective images. NeuroImage 45(4):1212–1219PubMedCrossRefGoogle Scholar
  53. Veldhuizen MG, Albrecht J, Zelano C, Boesveldt S, Breslin P, Lundstrom JN (2011) Identification of human gustatory cortex by activation likelihood estimation. Hum Brain Mapp 32(12):2256–2266PubMedCentralPubMedCrossRefGoogle Scholar
  54. Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3(4):255–274PubMedCrossRefGoogle Scholar
  55. Wager TD, Phan KL, Liberzon I, Taylor SE (2003) Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. NeuroImage 19:513–531PubMedCrossRefGoogle Scholar
  56. Wager TD, Jonides J, Reading S (2004) Neuroimaging studies of shifting attention: a meta-analysis. NeuroImage 22(4):1679–1693PubMedCrossRefGoogle Scholar
  57. Wessa M, Heissler J, Schonfelder S, Kanske P (2012) Goal-directed behavior under emotional distraction is preserved by enhanced task-specific activation. Soc Cogn Affect NeurosciGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Experimental Clinical and Health Psychology, Ghent UniversityGhentBelgium

Personalised recommendations