Animal Cognition

, Volume 19, Issue 3, pp 435–449 | Cite as

How chimpanzees (Pan troglodytes) perform in a modified emotional Stroop task

Original Paper

Abstract

The emotional Stroop task is an experimental paradigm developed to study the relationship between emotion and cognition. Human participants required to identify the color of words typically respond more slowly to negative than to neutral words (emotional Stroop effect). Here we investigated whether chimpanzees (Pan troglodytes) would show a comparable effect. Using a touch screen, eight chimpanzees were trained to choose between two simultaneously presented stimuli based on color (two identical images with differently colored frames). In Experiment 1, the images within the color frames were shapes that were either of the same color as the surrounding frame or of the alternative color. Subjects made fewer errors and responded faster when shapes were of the same color as the frame surrounding them than when they were not, evidencing that embedded images affected target selection. Experiment 2, a modified version of the emotional Stroop task, presented subjects with four different categories of novel images: three categories of pictures of humans (veterinarian, caretaker, and stranger), and control stimuli showing a white square. Because visits by the veterinarian that include anaesthetization can be stressful for subjects, we expected impaired performance in trials presenting images of the veterinarian. For the first session, we found correct responses to be indeed slower in trials of this category. This effect was more pronounced for subjects whose last anaesthetization experience was more recent, indicating that emotional valence caused the slowdown. We propose our modified emotional Stroop task as a simple method to explore which emotional stimuli affect cognitive performance in nonhuman primates.

Keywords

Chimpanzee Emotional Stroop Great apes Attentional bias Cognitive bias 

References

  1. Algom D, Chajut E, Lev S (2004) A rational look at the emotional Stroop phenomenon: a generic slowdown, not a stroop effect. J Exp Psychol Gen 133:323–338. doi:10.1037/0096-3445.133.3.323 CrossRefPubMedGoogle Scholar
  2. Bar-Haim Y, Lamy D, Pergamin L, Bakermans-Kranenburg MJ, Van Ijzendoorn MH (2007) Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychol Bull 133:1–24. doi:10.1037/0033-2909.133.1.1 CrossRefPubMedGoogle Scholar
  3. Bateson M, Nettle D (2015) Development of a cognitive bias methodology for measuring low mood in chimpanzees. PeerJ 3:e998. doi:10.7717/peerj.998 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ben-Haim MS, Mama Y, Icht M, Algom D (2014) Is the emotional Stroop task a special case of mood induction? Evidence from sustained effects of attention under emotion. Atten Percept Psychophys 76:81–97. doi:10.3758/s13414-013-0545-7 CrossRefPubMedGoogle Scholar
  5. Bethell EJ (2015) A “how-to” guide for designing judgment bias studies to assess captive animal welfare. J Appl Anim Welf Sci 18(sup1):18–42. doi:10.1080/10888705.2015.1075833 CrossRefGoogle Scholar
  6. Bethell EJ, Holmes A, Maclarnon A, Semple S (2012) Cognitive bias in a non-human primate: husbandry procedures influence cognitive indicators of psychological well-being in captive rhesus macaques. Anim Welf 21:185–195. doi:10.7120/09627286.21.2.185 CrossRefGoogle Scholar
  7. Bovet D, Vauclair J (2000) Picture recognition in animals and humans. Behav Brain Res 109:143–165. doi:10.1016/S0166-4328(00)00146-7 CrossRefPubMedGoogle Scholar
  8. Boysen ST, Berntson GG (1989) Conspecific recognition in the chimpanzee (Pan troglodytes): cardiac responses to significant others. J Comp Psychol 103:215–220. doi:10.1037/0735-7036.103.3.215 CrossRefPubMedGoogle Scholar
  9. Buckley TC, Blanchard EB, Neill WT (2000) Information processing and PTSD: a review of the empirical literature. Clin Psychol Rev 20:1041–1065. doi:10.1016/S0272-7358(99)00030-6 CrossRefPubMedGoogle Scholar
  10. Cohen J, Cohen P (1983) Applied multiple regression/correlation analysis for the behavioral sciences. Erlbaum, HillsdaleGoogle Scholar
  11. Constantine R, McNally RJ, Hornig CD (2001) Snake fear and the pictorial emotional Stroop paradigm. Cognit Ther Res 25:757–764. doi:10.1023/A:1012923507617 CrossRefGoogle Scholar
  12. De Ruiter C, Brosschot JF (1994) The emotional Stroop interference effect in anxiety: attentional bias or cognitive avoidance? Behav Res Ther 32:315–319. doi:10.1016/0005-7967(94)90128-7 CrossRefPubMedGoogle Scholar
  13. Fagot J, Martin-Malivel J, Dépy D (2000) What is the evidence for an equivalence between objects and pictures in birds and nonhuman primates. In: Fagot J (ed) Picture perception in animals. Psychology Press, New York, pp 295–320Google Scholar
  14. Field M, Cox WM (2008) Attentional bias in addictive behaviors: a review of its development, causes, and consequences. Drug Alcohol Depen 97:1–20. doi:10.1016/j.drugalcdep.2008.03.030 CrossRefGoogle Scholar
  15. Fox E, Griggs L, Mouchlianitis E (2007) The detection of fear-relevant stimuli: Are guns noticed as quickly as snakes? Emotion 7:691–696. doi:10.1037/1528-3542.7.4.691 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Frings C, Englert J, Wentura D, Bermeitinger C (2010) Decomposing the emotional Stroop effect. Q J Exp Psychol 63:42–49. doi:10.1080/17470210903156594 CrossRefGoogle Scholar
  17. Hirata S et al (2013) Brain response to affective pictures in the chimpanzee. Sci Rep. doi:10.1038/srep01342 Google Scholar
  18. Kano F, Tanaka M, Tomonaga M (2008) Enhanced recognition of emotional stimuli in the chimpanzee (Pan troglodytes). Anim Cogn 11:517–524. doi:10.1007/s10071-008-0142-7 CrossRefPubMedGoogle Scholar
  19. Kindt M, Brosschot JF (1997) Phobia-related cognitive bias for pictorial and linguistic stimuli. J Abnorm Psychol 106:644–648. doi:10.1037/0021-843X.106.4.644 CrossRefPubMedGoogle Scholar
  20. King JE, Figueredo AJ (1997) The five-factor model plus dominance in chimpanzee personality. J Res Pers 31:257–271. doi:10.1006/jrpe.1997.2179 CrossRefGoogle Scholar
  21. King HM, Kurdziel LB, Meyer JS, Lacreuse A (2012) Effects of testosterone on attention and memory for emotional stimuli in male rhesus monkeys. Psychoneuroendocrino 37:396–409. doi:10.1016/j.psyneuen.2011.07.010 CrossRefGoogle Scholar
  22. Koda H, Sato A, Kato A (2013) Is attentional prioritisation of infant faces unique in humans?: comparative demonstrations by modified dot-probe task in monkeys. Behav Process 98:31–36. doi:10.1016/j.beproc.2013.04.013 CrossRefGoogle Scholar
  23. Koster EH, Crombez G, Van Damme S, Verschuere B, De Houwer J (2004) Does imminent threat capture and hold attention? Emotion 4:312–317. doi:10.1037/1528-3542.4.3.312 CrossRefPubMedGoogle Scholar
  24. Lacreuse A, Schatz K, Strazzullo S, King HM, Ready R (2013) Attentional biases and memory for emotional stimuli in men and male rhesus monkeys. Anim Cogn 16:861–871. doi:10.1007/s10071-013-0618-y CrossRefPubMedGoogle Scholar
  25. Lang PJ, Davis M, Öhman A (2000) Fear and anxiety: animal models and human cognitive psychophysiology. J Affect Disord 61:137–159. doi:10.1016/S0165-0327(00)00343-8 CrossRefPubMedGoogle Scholar
  26. Lavy E, Van den Hout M (1993) Selective attention evidenced by pictorial and linguistic Stroop tasks. Behav Ther 24:645–657. doi:10.1016/S0005-7894(05)80323-5 CrossRefGoogle Scholar
  27. Mackay DG, Shafto M, Taylor JK, Marian DE, Abrams L, Dyer JR (2004) Relations between emotion, memory, and attention: evidence from taboo Stroop, lexical decision, and immediate memory tasks. Mem Cogn 32:474–488. doi:10.3758/BF03195840 CrossRefGoogle Scholar
  28. MacLeod C, Mathews A, Tata P (1986) Attentional bias in emotional disorders. J Abnorm Psychol 95:15–20. doi:10.1037//0021-843X.95.1.15 CrossRefPubMedGoogle Scholar
  29. Marzouki Y, Gullstrand J, Goujon A, Fagot J (2014) Baboons’ response speed is biased by their mood. PLoS ONE 9(7):e102562. doi:10.1371/journal.pone.0102562 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mathews A, MacLeod C (1985) Selective processing of threat cues in anxiety states. Behav Res Ther 23:563–569. doi:10.1016/0005-7967(85)90104-4 CrossRefPubMedGoogle Scholar
  31. Mauer N, Borkenau P (2007) Temperament and early information processing: temperament-related attentional bias in emotional Stroop tasks. Pers Indiv Differ 43:1063–1073. doi:10.1016/j.paid.2007.02.025 CrossRefGoogle Scholar
  32. McKenna FP, Sharma D (2004) Reversing the emotional Stroop effect reveals that it is not what it seems: the role of fast and slow components. J Exp Psychol Learn 30:382–392. doi:10.1037/0278-7393.30.2.382 CrossRefGoogle Scholar
  33. Mogg K, Bradley BP (2003) Selective processing of nonverbal information in anxiety: attentional biases for threat. In: Philippot P, Feldman RS, Coats EJ (eds) Nonverbal behavior in clinical settings. Oxford University Press, New York, pp 127–143CrossRefGoogle Scholar
  34. Öhman A, Mineka S (2001) Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol Rev 108:483–522. doi:10.1037/0033-295X.108.3.483 CrossRefPubMedGoogle Scholar
  35. Parr LA (2001) Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes). Anim Cogn 4:223–229. doi:10.1007/s100710100085 CrossRefPubMedGoogle Scholar
  36. Paul ES, Harding EJ, Mendl M (2005) Measuring emotional processes in animals: the utility of a cognitive approach. Neurosci Biobehav Rev 29:469–491. doi:10.1016/j.neubiorev.2005.01.002 CrossRefPubMedGoogle Scholar
  37. Phaf RH, Kan K-J (2007) The automaticity of emotional Stroop: a meta-analysis. J Behav Ther Exp Psy 38:184–199. doi:10.1016/j.jbtep.2006.10.008 CrossRefGoogle Scholar
  38. Pomerantz O, Terkel J, Suomi SJ, Paukner A (2012) Stereotypic head twirls, but not pacing, are related to a ‘pessimistic’-like judgment bias among captive tufted capuchins (Cebus apella). Anim Cogn 15:689–698. doi:10.1007/s10071-012-0497-7 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Pratto F, John OP (1991) Automatic vigilance: the attention-grabbing power of negative social information. J Pers Soc Psychol 61:380–391. doi:10.1037/0022-3514.61.3.380 CrossRefPubMedGoogle Scholar
  40. Robbins SJ, Ehrman RN (2004) The role of attentional bias in substance abuse. Behav Cogn Neurosci Rev 3:243–260. doi:10.1177/1534582305275423 CrossRefPubMedGoogle Scholar
  41. Schmidt LJ, Belopolsky AV, Theeuwes J (2014) Attentional capture by signals of threat. Cogn Emot. doi:10.1080/02699931.2014.924484 PubMedGoogle Scholar
  42. Shibasaki M, Kawai N (2009) Rapid detection of snakes by Japanese monkeys (Macaca fuscata): an evolutionarily predisposed visual system. J Comp Psychol 123:131–135. doi:10.1037/a0015095 CrossRefPubMedGoogle Scholar
  43. Shibasaki M, Isomura T, Masataka N (2014) Viewing images of snakes accelerates making judgements of their colour in humans: red snake effect as an instance of ‘emotional Stroop facilitation’. R Soc Open Sci. doi:10.1098/rsos.140066 PubMedPubMedCentralGoogle Scholar
  44. Siegrist M (1995) Effects of taboo words on color-naming performance on a Stroop test. Percept Motor Skill 81:1119–1122. doi:10.2466/pms.1995.81.3f.1119 CrossRefGoogle Scholar
  45. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  46. Waters AJ, Sayette MA, Wertz JM (2003) Carry-over effects can modulate emotional Stroop effects. Cogn Emot 17:501–509. doi:10.1080/02699930143000716 CrossRefGoogle Scholar
  47. Weiss A et al (2009) Assessing chimpanzee personality and subjective well-being in Japan. Am J Primatol 71:283–292. doi:10.1002/ajp.20649 CrossRefPubMedGoogle Scholar
  48. Williams JMG, Mathews A, MacLeod C (1996) The emotional Stroop task and psychopathology. Psychol Bull 120:3–24. doi:10.1037/0033-2909.120.1.3 CrossRefPubMedGoogle Scholar
  49. Witthöft M, Rist F, Bailer J (2008) Enhanced early emotional intrusion effects and proportional habituation of threat response for symptom and illness words in college students with elevated health anxiety. Cogn Ther Res 32:818–842. doi:10.1007/s10608-007-9159-5 CrossRefGoogle Scholar
  50. Yiend J (2010) The effects of emotion on attention: a review of attentional processing of emotional information. Cogn Emot 24:3–47. doi:10.1080/02699930903205698 CrossRefGoogle Scholar
  51. Yiend J, Barnicot K, Koster EH (2013) Attention and emotion. In: Robinson MD, Watkins ER, Harmon-Jones E (eds) Handbook of cognition and emotion. Guilford Press, New York, pp 97–116Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Matthias Allritz
    • 1
    • 2
  • Josep Call
    • 2
    • 3
  • Peter Borkenau
    • 1
  1. 1.Department for Differential Psychology and Psychological AssessmentMartin Luther University Halle-WittenbergHalle (Saale)Germany
  2. 2.Department of Developmental and Comparative PsychologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany
  3. 3.School of Psychology and NeuroscienceUniversity of St AndrewsSt AndrewsUK

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