Cognitive Processing

, Volume 19, Issue 1, pp 125–132 | Cite as

Only “efficient” emotional stimuli affect the content of working memory during free-recollection from natural scenes

  • Arianna Buttafuoco
  • Tiziana Pedale
  • Tony W. Buchanan
  • Valerio Santangelo
Short Communication

Abstract

Emotional events are thought to have privileged access to attention and memory, consuming resources needed to encode competing emotionally neutral stimuli. However, it is not clear whether this detrimental effect is automatic or depends on the successful maintenance of the specific emotional object within working memory. Here, participants viewed everyday scenes including an emotional object among other neutral objects followed by a free-recollection task. Results showed that emotional objects—irrespective of their perceptual saliency—were recollected more often than neutral objects. The probability of being recollected increased as a function of the arousal of the emotional objects, specifically for negative objects. Successful recollection of emotional objects (positive or negative) from a scene reduced the overall number of recollected neutral objects from the same scene. This indicates that only emotional stimuli that are efficient in grabbing (and then consuming) available attentional resources play a crucial role during the encoding of competing information, with a subsequent bias in the recollection of neutral representations.

Keywords

Emotion Salience Working memory Capacity Free recollection 

Notes

Acknowledgements

The study has been partially funded by the Russian Academic Excellence Project ‘5-100’.

References

  1. Anderson AK, Phelps EA (2001) Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 411:305–309.  https://doi.org/10.1038/35077083 CrossRefPubMedGoogle Scholar
  2. Bannerman RL, Temminck EV, Sahraie A (2012) Emotional stimuli capture spatial attention but do not modulate spatial memory. Vis Res 65:12–20.  https://doi.org/10.1016/j.visres.2012.05.011 CrossRefPubMedGoogle Scholar
  3. Beaman CP, Morton J (2000) The separate but related origins of the recency effect and the modality effect in free recall. Cognition 77:B59–B65.  https://doi.org/10.1016/S0010-0277(00)00107-4 CrossRefPubMedGoogle Scholar
  4. Bradley MM (2009) Natural selective attention: orienting and emotion. Psychophysiology 46:1–11.  https://doi.org/10.1111/j.1469-8986.2008.00702.x CrossRefPubMedGoogle Scholar
  5. Brainerd CJ, Reyna VF, Howe ML, Kevershan J (1990) The last shall be first: how memory strength affects children’s retrieval. Psychol Sci 1:247–252.  https://doi.org/10.1111/j.1467-9280.1990.tb00208.x CrossRefGoogle Scholar
  6. Buchanan TW, Adolphs R (2002) The role of the human amygdala in emotional modulation of long-term declarative memory. In: Moore S, Oaksford M (eds) Emotional cognition: from brain to behavior. John Benjamins, London, pp 9–34CrossRefGoogle Scholar
  7. Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Ann Rev Neurosci 18:193–222.  https://doi.org/10.1146/annurev.ne.18.030195.001205 CrossRefPubMedGoogle Scholar
  8. Dolcos F, McCarthy G (2006) Brain systems mediating cognitive interference by emotional distraction. J Neurosci 26:2072–2079.  https://doi.org/10.1523/JNEUROSCI.5042-05.2006 CrossRefPubMedGoogle Scholar
  9. Hurlstone MJ, Hitch GJ, Baddeley AD (2014) Memory for serial order across domains: an overview of the literature and directions for future research. Psychol Bull 140:339.  https://doi.org/10.1037/a0034221 CrossRefPubMedGoogle Scholar
  10. Itti L, Koch C, Niebur E (1998) A model of saliency-based visual attention for rapid scene analysis. IEEE Trans Pattern Anal Mach Intell 20:1254–1259.  https://doi.org/10.1109/34.730558 CrossRefGoogle Scholar
  11. Katkov M, Romani S, Tsodyks M (2015) Effects of long-term representations on free recall of unrelated words. Learn Mem 22:101–108.  https://doi.org/10.1101/lm.035238.114 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Kensinger EA, Corkin S (2003) Effect of negative emotional content on working memory and long-term memory. Emotion 3:378.  https://doi.org/10.1037/1528-3542.3.4.378 CrossRefPubMedGoogle Scholar
  13. Kensinger EA, Corkin S (2004) Two routes to emotional memory: distinct neural processes for valence and arousal. Proc Natl Acad Sci USA 101:3310–3315.  https://doi.org/10.1073/pnas.0306408101 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kim JSC, Vossel G, Gamer M (2013) Effects of emotional context on memory for details: the role of attention. PLoS ONE 8:e77405.  https://doi.org/10.1371/journal.pone.0077405 CrossRefPubMedPubMedCentralGoogle Scholar
  15. LaBar KS, Cabeza R (2006) Cognitive neuroscience of emotional memory. Nat Rev Neurosci 7:54–64.  https://doi.org/10.1038/nrn1825 CrossRefPubMedGoogle Scholar
  16. Lang PJ, Bradley MM, Cuthbert BN (2005) International affective picture system (IAPS): affective ratings of pictures and instruction manual. Technical report A-6. University of Florida, Gainesville, FLGoogle Scholar
  17. 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 18:614–625.  https://doi.org/10.1162/jocn.2006.18.4.614 CrossRefPubMedGoogle Scholar
  18. Melcher D (2010) Accumulating and remembering the details of neutral and emotional natural scenes. Perception 39:1011–1025.  https://doi.org/10.1068/p6670 CrossRefPubMedGoogle Scholar
  19. Nardo D, Santangelo V, Macaluso E (2011) Stimulus-driven orienting of visuo-spatial attention in complex dynamic environments. Neuron 69:1015–1028.  https://doi.org/10.1016/j.neuron.2011.02.020 CrossRefPubMedGoogle Scholar
  20. Pedale T, Santangelo V (2015) Perceptual salience affects the contents of working memory during free-recollection of objects from natural scenes. Front Hum Neurosci 9:60.  https://doi.org/10.3389/fnhum.2015.00060 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Pedale T, Basso D, Santangelo V (2017) Processing of negative stimuli facilitates event-based prospective memory only under low memory load. J Cogn Psychol.  https://doi.org/10.1080/20445911.2017.1329204 Google Scholar
  22. Perlstein WM, Elbert T, Stenger VA (2002) Dissociation in human prefrontal cortex of affective influences on working memory-related activity. Proc Natl Acad Sci 99:1736–1741.  https://doi.org/10.1073/pnas.241650598 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Pourtois G, Schettino A, Vuilleumier P (2013) Brain mechanisms for emotional influences on perception and attention: what is magic and what is not. Biol Psychol 92:492–512.  https://doi.org/10.1016/j.biopsycho.2012.02.007 CrossRefPubMedGoogle Scholar
  24. Sakaki M, Fryer K, Mather M (2014) Emotion strengthens high-priority memory traces but weakens low-priority memory traces. Psychol Sci 25:387–395.  https://doi.org/10.1177/0956797613504784 CrossRefPubMedGoogle Scholar
  25. Santangelo V (2015) Forced to remember: when memory is biased by salient information. Behav Brain Res 283:1–10.  https://doi.org/10.1016/j.bbr.2015.01.013 CrossRefPubMedGoogle Scholar
  26. Santangelo V, Macaluso E (2013) Visual salience improves spatial working memory via enhanced parieto-temporal functional connectivity. J Neurosci 33:4110–4117.  https://doi.org/10.1523/JNEUROSCI.4138-12.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Simione L, Calabrese L, Marucci FS, Belardinelli MO, Raffone A, Maratos FA (2014) Emotion based attentional priority for storage in visual short-term memory. PLoS ONE 9:e95261.  https://doi.org/10.1371/journal.pone.0095261 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Standing L (1973) Learning 10000 pictures. Q J Exp Psychol 25:207–222.  https://doi.org/10.1080/14640747308400340 CrossRefPubMedGoogle Scholar
  29. Steinmetz KRM, Addis DR, Kensinger EA (2010) The effect of arousal on the emotional memory network depends on valence. Neuroimage 53:318–324.  https://doi.org/10.1016/j.neuroimage.2010.06.015 CrossRefGoogle Scholar
  30. Tan L, Ward G (2007) Output order in immediate serial recall. Mem Cogn 35:1093–1106.  https://doi.org/10.3758/BF03193481 CrossRefGoogle Scholar
  31. Vuilleumier P (2005) How brains beware: neural mechanisms of emotional attention. Trends Cogn Sci 9:585–594.  https://doi.org/10.1016/j.tics.2005.10.011 CrossRefPubMedGoogle Scholar
  32. Yiend J (2010) The effects of emotion on attention: a review of attentional processing of emotional information. Cogn Emot 24:3–47.  https://doi.org/10.1080/02699930903205698 CrossRefGoogle Scholar

Copyright information

© Marta Olivetti Belardinelli and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Arianna Buttafuoco
    • 1
  • Tiziana Pedale
    • 2
    • 3
    • 4
  • Tony W. Buchanan
    • 5
  • Valerio Santangelo
    • 1
    • 4
  1. 1.Department of Philosophy, Social Sciences and EducationUniversity of PerugiaPerugiaItaly
  2. 2.Centre for Cognition and Decision MakingNational Research University - Higher School of EconomicsMoscowRussian Federation
  3. 3.Department of PsychologySapienza University of RomeRomeItaly
  4. 4.Neuroimaging LaboratorySanta Lucia FoundationRomeItaly
  5. 5.Department of PsychologySaint Louis UniversitySaint LouisUSA

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