Abstract
At the start of the new millennium, the “cognitive bias” paradigm emerged as a new approach to assessing animal emotion. In the animal welfare literature, cognitive bias describes how emotions such as anxiety and depression are associated with changes in the way the brain processes information. For example, studies with humans have long demonstrated that anxious people are more vigilant for negative cues and depressed people interpret the proverbial glass of water as “half empty” rather than “half full.” In this chapter, we review how methods developed to study cognitive bias in humans have been adapted to measure the interaction between emotion and cognition in nonhuman primates. We focus on judgment bias and attention bias tasks and discuss study design, controls, confounds, and advantages and limitations of each. We also indicate future research directions. This chapter is intended to introduce readers with little or no experience of cognitive bias tasks to theory and practical considerations around designing these tasks.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Allritz M, Call J, Borkenau P (2016) How chimpanzees (Pan troglodytes) perform in a modified emotional Stroop task. Anim Cogn 19:435–449. https://doi.org/10.1007/s10071-015-0944-3
Bar-Haim Y, Lamy D, Pergamin L et al (2007) Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychol Bull 133(1):1–24. https://doi.org/10.1037/0033-2909.133.1.1
Bateson M, Nettle D (2015) Development of a cognitive bias methodology for measuring low mood in chimpanzees. PeerJ 3:e998. https://doi.org/10.7717/peerj.998
Beevers CG, Gibb BE, McGeary JE, Miller IW (2007) Serotonin transporter genetic variation and biased attention for emotional word stimuli among psychiatric inpatients. J Abnorm Psychol 116(1):208–212. https://doi.org/10.1037/0021-843X.116.1.208
Bethell EJ (2015) A “how-to” guide for designing judgment bias studies to assess captive animal welfare. J Appl Anim Welf Sci 18(S1):S18–S42. https://doi.org/10.1080/10888705.2015.1075833
Bethell EJ, Koyama NF (2015) Happy hamsters? Enrichment induces positive judgement bias for mildly (but not truly) ambiguous cues to reward and punishment in Mesocricetus auratus. R Soc Open Sci 2(7):140399. https://doi.org/10.1098/rsos.140399
Bethell EJ, Holmes A, MacLarnon A, Semple S (2012a) Cognitive bias in a non-human primate: husbandry procedures influence cognitive indicators of psychological well-being in captive rhesus macaques. Anim Welf 21(2):185–195. https://doi.org/10.7120/09627286.21.2.185
Bethell EJ, Holmes A, MacLarnon A, Semple S (2012b) Evidence that emotion mediates social attention in rhesus macaques. PLoS One 7(8):e44387. https://doi.org/10.1371/journal.pone.0044387
Bethell EJ, Holmes A, MacLarnon A, Semple S (2016) Emotion evaluation and response slowing in a non-human primate: new directions for cognitive bias measures of animal emotion? Behav Sci 6(1):2. https://doi.org/10.3390/bs6010002
Bethell EJ, Kemp C, Thatcher H et al (2019a) Heritability and maternal effects on social attention during an attention bias task in a non-human primate, Macaca mulatta. EcoEvoRxiv Prepr. https://doi.org/10.32942/osf.io/5nzd4
Bethell EJ, Cassidy LC, Brockhausen RR, Pfefferle D (2019b) Toward a standardized test of fearful temperament in primates: a sensitive alternative to the human intruder task for laboratory-housed rhesus macaques (Macaca mulatta). Front Psychol 10:1051. https://doi.org/10.3389/fpsyg.2019.01051
Bradley BP, Mogg K, Falla SJ, Hamilton LR (1998) Attentional bias for threatening facial expressions in anxiety: manipulation of stimulus duration. Cogn Emot 12(6):737–753. https://doi.org/10.1080/026999398379411
Broom DM (2010) Cognitive ability and awareness in domestic animals and decisions about obligations to animals. Appl Anim Behav Sci 126(1–2):1–11. https://doi.org/10.1016/j.applanim.2010.05.001
Calvo MG, Avero P (2005) Time course of attentional bias to emotional scenes in anxiety: Gaze direction and duration. Cogn Emot 19(3):433–451. https://doi.org/10.1080/02699930441000157
Carlson JM, Mujica-Parodi LR, Harmon-Jones E, Hajcak G (2012) The orienting of spatial attention to backward masked fearful faces is associated with variation in the serotonin transporter gene. Emotion 12(2):203–207. https://doi.org/10.1037/a0025170
Chen NTM, Clarke PJF (2017) Gaze-based assessments of vigilance and avoidance in social anxiety: a review. Curr Psychiatry Rep 19:59. https://doi.org/10.1007/s11920-017-0808-4
Chen Y, Ehlers A, Clark D, Mansell W (2002) Patients with generalized social phobia direct their attention away from faces. Behav Res Ther 40(6):677–687. https://doi.org/10.1016/S0005-7967(01)00086-9
Clark DM (1999) Anxiety disorders: why they persist and how to treat them. Behav Res Ther 37(S1):S5–S27. https://doi.org/10.1016/S0005-7967(99)00048-0
Cronin KA, Bethell EJ, Jacobson SL, Egelkamp C, Hopper LM, Ross SR (2018) Evaluating mood changes in response to anthropogenic noise with a response-slowing task in three species of zoo-housed primates. Anim Behav Cogn 5(2):209–221. https://doi.org/10.26451/abc.05.02.03.2018
Crump A, Arnott G, Bethell E (2018) Affect-driven attention biases as animal welfare indicators: review and methods. Animals 8(8):136. https://doi.org/10.3390/ani8080136
Crump A, Bethell EJ, Earley R, Lee VE, Mendl M, Oldham L, Turner SP, Arnott G (2020) Emotion in animal contests. Proc R Soc B Biol Sci 287(1939):20201715. https://doi.org/10.1098/rspb.2020.1715
Dawkins MS (2017) Animal welfare with and without consciousness. J Zool 301(1):1–10. https://doi.org/10.1111/jzo.12434
de Waal FBM (2006) Primates and philosophers: how morality evolved. Princeton, Princeton Science Library
Evans JSBT (2008) Dual-processing accounts of reasoning, judgment, and social cognition. Annu Rev Psychol 59:255–278. https://doi.org/10.1146/annurev.psych.59.103006.093629
Garner M, Mogg K, Bradley BP (2006) Orienting and maintenance of gaze to facial expressions in social anxiety. J Abnorm Psychol 115(4):760–770. https://doi.org/10.1037/0021-843X.115.4.760
Gerald MS, Waitt C, Little AC (2009) Pregnancy coloration in macaques may act as a warning signal to reduce antagonism by conspecifics. Behav Process 80(1):7–11. https://doi.org/10.1016/j.beproc.2008.08.001
Gilboa-Schechtman E, Foa EB, Amir N (1999) Attentional biases for facial expressions in social phobia: the face-in-the-crowd paradigm. Cogn Emot 13(3):305–318. https://doi.org/10.1080/026999399379294
Goodall J (1986) The chimpanzees of Gombe: patterns of behaviour. Harvard University Press, Cambridge
Gordon DJ, Rogers LJ (2015) Cognitive bias, hand preference and welfare of common marmosets. Behav Brain Res 287:100–108. https://doi.org/10.1016/j.bbr.2015.03.037
Harding EJ, Paul ES, Mendl M (2004) Cognitive bias and affective state. Nature 427:312. https://doi.org/10.1038/427312a
Hommer RE, Meyer A, Stoddard J et al (2014) Attention bias to threat faces in severe mood dysregulation. Depress Anxiety 31(7):559–565. https://doi.org/10.1002/da.22145
Kano F, Tomonaga M (2010) Attention to emotional scenes including whole-body expressions in chimpanzees (Pan troglodytes). J Comp Psychol 124(3):287–294. https://doi.org/10.1037/a0019146
Kawai N, Koda H (2016) Japanese monkeys (Macaca fuscata) quickly detect snakes but not spiders: evolutionary origins of fear-relevant animals. J Comp Psychol 130(3):299–303. https://doi.org/10.1037/com0000032
Kawai N, Kubo K, Masataka N, Hayakawa S (2016) Conserved evolutionary history for quick detection of threatening faces. Anim Cogn 19:655–660. https://doi.org/10.1007/s10071-015-0949-y
King HM, Kurdziel LB, Meyer JS, Lacreuse A (2012) Effects of testosterone on attention and memory for emotional stimuli in male rhesus monkeys. Psychoneuroendocrinology 37(3):396–409. https://doi.org/10.1016/j.psyneuen.2011.07.010
Kret ME, Jaasma L, Bionda T, Wijnen JG (2016) Bonobos (Pan paniscus) show an attentional bias toward conspecifics’ emotions. Proc Natl Acad Sci U S A 113(14):3761–3766. https://doi.org/10.1073/pnas.1522060113
Lang PJ, Davis M, Öhman A (2000) Fear and anxiety: animal models and human cognitive psychophysiology. J Affect Disord 61(3):137–159. https://doi.org/10.1016/S0165-0327(00)00343-8
LeDoux J (1996) The emotional brain: the mysterious underpinnings of emotional life. Simon & Schuster, New York
Lindell AK (2013) Continuities in emotion lateralization in human and non-human primates. Front Hum Neurosci 7:464. https://doi.org/10.3389/fnhum.2013.00464
MacLeod C, Mathews A, Tata P (1986) Attentional bias in emotional disorders. J Abnorm Psychol 95(1):15–20. https://doi.org/10.1037/0021-843X.95.1.15
MacLeod C, Rutherford E, Campbell L et al (2002) Selective attention and emotional vulnerability: assessing the causal basis of their association through the experimental manipulation of attentional bias. J Abnorm Psychol 111(1):107–123. https://doi.org/10.1037/0021-843X.111.1.107
Mandalaywala TM, Bethell EJ, Parker KJ, Maestripieri D (2013) Negativity bias in free-ranging infant rhesus macaques (Macaca mulatta) on Cayo Santiago, Puerto Rico. Am J Primatol 75(S1):43. https://doi.org/10.1002/ajp.22188
Mandalaywala TM, Parker KJ, Maestripieri D (2014) Early experience affects the strength of vigilance for threat in rhesus monkey infants. Psychol Sci 25(10):1893–1902. https://doi.org/10.1177/0956797614544175
Mathews A (1990) Why worry? The cognitive function of anxiety. Behav Res Ther 28(6):455–468. https://doi.org/10.1016/0005-7967(90)90132-3
Mathews A, MacLeod C (2005) Cognitive vulnerability to emotional disorders. Annu Rev Clin Psychol 1:167–195. https://doi.org/10.1146/annurev.clinpsy.1.102803.143916
McGuire MC, Vonk J, Fuller G, Allard S (2017) Using an ambiguous cue paradigm to assess cognitive bias in gorillas (Gorilla gorilla gorilla) during a forage manipulation. Anim Behav Cogn 4(1):91–104. https://doi.org/10.12966/abc.06.02.2017
Mendl M (1999) Performing under pressure: stress and cognitive function. Appl Anim Behav Sci 65(3):221–244. https://doi.org/10.1016/S0168-1591(99)00088-X
Mendl M, Paul ES (2004) Consciousness, emotion and animal welfare: insights from cognitive science. Anim Welf 13(Suppl):S17–S25
Mendl MT, Burman OHP, Parker RMA, Paul ES (2009) Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Appl Anim Behav Sci 118(3–4):161–181. https://doi.org/10.1016/j.applanim.2009.02.023
Mogg K, Bradley BP (1999) Orienting of attention to threatening facial expressions presented under conditions of restricted awareness. Cogn Emot 13(6):713–740. https://doi.org/10.1080/026999399379050
Mogg K, Bradley BP, Miles F, Dixon R (2004) Time course of attentional bias for threat scenes: Testing the vigilance-avoidance hypothesis. Cogn Emot 18(5):689–700. https://doi.org/10.1080/02699930341000158
Neville V, Nakagawa S, Zidar J et al (2020) Pharmacological manipulations of judgement bias: a systematic review and meta-analysis. Neurosci Biobehav Rev 108:269–286. https://doi.org/10.1016/j.neubiorev.2019.11.008
Öhman A, Mineka S (2003) The malicious serpent: snakes as a prototypical stimulus for an evolved module of fear. Curr Dir Psychol Sci 12(1):5–9. https://doi.org/10.1111/1467-8721.01211
Öhman A, Flykt A, Esteves F (2001) Emotion drives attention: detecting the snake in the grass. J Exp Psychol Gen 130(3):466–478. https://doi.org/10.1037/0096-3445.130.3.466
Panksepp J (1998) Affective neuroscience: the foundations of human and animal emotions. Oxford University Press, New York
Panksepp J (2011) The basic emotional circuits of mammalian brains: do animals have affective lives? Neurosci Biobehav Rev 35(9):1791–1804. https://doi.org/10.1016/j.neubiorev.2011.08.003
Panksepp J (2014) Integrating bottom-up internalist views of emotional feelings with top-down externalist views: might brain affective changes constitute reward and punishment effects within animal brains? Cortex 59:208–213. https://doi.org/10.1016/j.cortex.2014.04.015
Parr LA (2011) The evolution of face processing in primates. Philos Trans R Soc B Biol Sci 366(1571):1764–1777. https://doi.org/10.1098/rstb.2010.0358
Parr LA, Hopkins W (2000) Brain temperature asymmetries and emotional perception in chimpanzees, Pan troglodytes. Physiol Behav 71(3–4):363–371. https://doi.org/10.1016/S0031-9384(00)00349-8
Parr LA, Murphy L, Feczko E et al (2016) Experience-dependent changes in the development of face preferences in infant rhesus monkeys. Dev Psychobiol 58(8):1002–1018. https://doi.org/10.1002/dev.21434
Perdue B (2017) Mechanisms underlying cognitive bias in nonhuman primates. Anim Behav Cogn 4(1):105–118. https://doi.org/10.12966/abc.08.02.2017
Pfefferle D (2020) Facial Stimuli - Macaques. figshare. Dataset. https://doi.org/10.6084/m9.figshare.13227779
Pfefferle D, Kazem AJN, Brockhausen RR et al (2014) Monkeys spontaneously discriminate their unfamiliar paternal kin under natural conditions using facial cues. Curr Biol 24(15):1806–1810. https://doi.org/10.1016/j.cub.2014.06.058
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. https://doi.org/10.1007/s10071-012-0497-7
Rosenthal R (1979) The file drawer problem and tolerance for null results. Psychol Bull 86(3):638–641. https://doi.org/10.1037/0033-2909.86.3.638
Russell W, Burch R (1959) The principles of humane experimental technique. Methuen & Co, London
Sato W, Aoki S (2006) Right hemispheric dominance in processing of unconscious negative emotion. Brain Cogn 62(3):261–266. https://doi.org/10.1016/j.bandc.2006.06.006
Schino G, Massimei R, Pinzaglia M, Addessi E (2016) Grooming, social rank and ‘optimism’ in tufted capuchin monkeys: a study of judgement bias. Anim Behav 119:11–16. https://doi.org/10.1016/j.anbehav.2016.06.017
Seligman MEP, Csikszentmihalyi M (2000) Positive psychology: an introduction. Am Psychol 55(1):5–14. https://doi.org/10.1037/0003-066X.55.1.5
Shibasaki M, Kawai N (2009) Rapid detection of snakes by Japanese monkeys (Macaca fuscata): an evolutionarily predisposed visual system. J Comp Psychol 123(2):131–135. https://doi.org/10.1037/a0015095
Tversky A, Kahneman D (1974) Judgment under uncertainty: heuristics and biases. Science 185(4157):1124–1131. https://doi.org/10.1126/science.185.4157.1124
van Rooijen R, Ploeger A, Kret ME (2017) The dot-probe task to measure emotional attention: a suitable measure in comparative studies? Psychon Bull Rev 24:1686–1717. https://doi.org/10.3758/s13423-016-1224-1
Waitt C, Buchanan-Smith HM (2006) Perceptual considerations in the use of colored photographic and video stimuli to study nonhuman primate behavior. Am J Primatol 68(11):1054–1067. https://doi.org/10.1002/ajp.20303
Waitt C, Little AC, Wolfensohn SE et al (2003) Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proc R Soc London B Biol Sci 270(Suppl_2):S144–S146. https://doi.org/10.1098/rsbl.2003.0065
Watson KK, Ghodasra JH, Furlong MA, Platt ML (2012) Visual preferences for sex and status in female rhesus macaques. Anim Cogn 15:401–407. https://doi.org/10.1007/s10071-011-0467-5
Williams JMG, Mathews A, MacLeod C (1996) The emotional Stroop task and psychopathology. Psychol Bull 120(1):3–24. https://doi.org/10.1037/0033-2909.120.1.3
Wilson DA, Tomonaga M (2018) Exploring attentional bias towards threatening faces in chimpanzees using the dot probe task. PLoS One 13(11):e0207378. https://doi.org/10.1371/journal.pone.0207378
Witham C, Bethell EJ (2019) Macaque faces. figshare. Dataset. https://doi.org/10.6084/m9.figshare.9862586
Yiend J (2010) The effects of emotion on attention: a review of attentional processing of emotional information. Cogn Emot 24(1):3–47. https://doi.org/10.1080/02699930903205698
Acknowledgments
We thank the funders of our research: NC3Rs (grant#: NC/L000539/1), European Cooperation in Science and Technology (COST) primTRAIN program (http://www.cost.eu/COST_Actions/ca/CA15131,COSTSTSMCA15131-36153), Leibniz-Science Campus Primate Cognition (https://www.primate-cognition.eu/en/funding-measures.html), German Research Foundation (https://www.dfg.de/) Research Unit 2591, the Primate Society of Great Britain, and the Universities Federation for Animal Welfare. We thank all of our collaborators, the Caribbean Primate Research Centre, and MRC Harwell Centre for Macaques for supporting our work. We also thank the editors and reviewers for their thoughtful comments on an earlier draft of this chapter. This chapter is dedicated to the memory of Jaak Panksepp and Corri Waitt.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Bethell, E.J., Pfefferle, D. (2023). Cognitive Bias Tasks: A New Set of Approaches to Assess Welfare in Nonhuman Primates. In: Robinson, L.M., Weiss, A. (eds) Nonhuman Primate Welfare. Springer, Cham. https://doi.org/10.1007/978-3-030-82708-3_9
Download citation
DOI: https://doi.org/10.1007/978-3-030-82708-3_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-82707-6
Online ISBN: 978-3-030-82708-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)