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Cognitive bias in a non-human primate: husbandry procedures influence cognitive indicators of psychological well-being in captive rhesus macaques

Published online by Cambridge University Press:  01 January 2023

EJ Bethell ,
A Holmes ,
A MacLarnon  and
S Semple
EJ Bethell*
Affiliation:
School of Natural Sciences and Psychology, James Parsons Building, Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, UK Department of Life Sciences, University of Roehampton, London SW15 4JD, UK
A Holmes
Affiliation:
Department of Psychology, University of Roehampton, London SW15 4JD, UK
A MacLarnon
Affiliation:
Department of Life Sciences, University of Roehampton, London SW15 4JD, UK
S Semple
Affiliation:
Department of Life Sciences, University of Roehampton, London SW15 4JD, UK
*
* Contact for correspondence and requests for reprints: [email protected]
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Abstract

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The measurement of ‘cognitive bias’ has recently emerged as a powerful tool for assessing animal welfare. Cognitive bias was initially, and widely, studied in humans, and describes the way in which particular emotions are associated with biases in information processing. People suffering from clinical levels of anxiety or depression, for example, interpret ambiguous events more negatively than do non-anxious or non-depressed people. Development of methods for use with non-human animals has revealed similar biases in several species of mammals and birds, and one invertebrate. However, cognitive bias has not been previously explored in any species of non-human primate, despite specific concerns raised about the welfare of these animals in captivity. Here, we describe a touchscreen-based cognitive-bias task developed for use with captive rhesus macaques (Macaca mulatta). Monkeys were initially trained on a ‘Go/No-Go’ operant task, in which they learned to touch one of two lines that differed in size in order to receive a reward (food), and to desist from touching the other line to avoid a mildly aversive stimulus (delay to the next trial and white noise). In testing sessions, the monkeys were presented with lines of intermediate size. We measured whether touchscreen responses to these ambiguous stimuli were affected by husbandry procedures (environmental enrichment, and a statutory health check involving restraint and ketamine hydrochloride injection) presumed to induce positive and negative shifts in affective state, respectively. Monkeys made fewer responses to ambiguous stimuli post health check compared to during the phase of enrichment suggesting greater expectation of negative outcomes following the health check compared to during enrichment. Shifts in affective state following standard husbandry procedures may therefore be associated with changes in information processing similar to those demonstrated in anxious and depressed humans, and in a number of other taxa.

Keywords

animal welfarecaptureemotionenrichmenthusbandry proceduresrhesus macaque
Type
Research Article
Information
Animal Welfare , Volume 21 , Issue 2 , May 2012 , pp. 185 - 195
Copyright
© 2012 Universities Federation for Animal Welfare

References

Bar-Haim, Y, Lamy, D, Pergamin, L, Bakermans-Kranenburg, MJ and van Ijzendoorn, MH 2007 Threat-related attentional bias in anxious and non-anxious individuals: a meta-analytic study. Psychological Bulletin 133: 1–24. http://dx.doi.org/10.1037/0033-2909.133.1.1CrossRefGoogle Scholar
Bateson, M and Matheson, SM 2007 Performance on a categorisation task suggests that removal of environmental enrichment induces ‘pessimism’ in captive European starlings (Sturnus vulgaris). Animal Welfare 16: 33–36Google Scholar
Bateson, M, Desire, S, Gartside, SE and Wright, GA 2011 Agitated honeybees exhibit pessimistic cognitive biases. Current Biology 2: 1070–1073. http://dx.doi.org/10.1016/j.cub.2011.05.017Google Scholar
Blanchette, I, Richards, A and Cross, A 2007 Anxiety and the interpretation of ambiguous facial expressions: the influence of contextual cues. Quarterly Journal of Experimental Psychology 60: 1101–1115. http://dx.doi.org/10.1080/17470210600890511CrossRefGoogle ScholarPubMed
Boissy, A, Manteuffel, G, Jensen, MB, Moe, RO, Spruijt, B, Keeling, LJ, Winckler, C, Forkman, B, Dimitrov, I, Langbein, J, Bakken, M, Veissier, I and Aubert, A 2007 Assessment of positive emotions in animals to improve their welfare. Physiology & Behavior 92: 375–397. http://dx.doi.org/10.1016/j.physbeh.2007.02.003Google ScholarPubMed
Brilot, BO, Asher, L and Bateson, M 2010 Stereotyping starlings are more ‘pessimistic’. Animal Cognition 13: 721–731. http://dx.doi.org/10.1007/s10071-010-0323-zCrossRefGoogle ScholarPubMed
Broom, DM 2010 Cognitive ability and awareness in domestic animals and decisions about obligations to animals. Applied Animal Behaviour Science 126: 1–11. http://dx.doi.org/10.1016/j.applanim.2010.05.001CrossRefGoogle Scholar
Brydges, NM, Leach, M, Nicol, K, Wright, R and Bateson, M 2011 Environmental enrichment induces optimistic cognitive bias in rats. Animal Behaviour 81: 169–175. http://dx.doi.org/10.1016/j.anbehav.2010.09.030CrossRefGoogle Scholar
Burman, OHP, Parker, RMA, Paul, ES and Mendl, M 2008a A spatial judgement task to determine background emotional state in laboratory rats, Rattus norvegicus. Animal Behaviour 76: 801–809. http://dx.doi.org/10.1016/j.anbehav.2008.02.014CrossRefGoogle Scholar
Burman, OHP, Parker, RMA, Paul, ES and Mendl, M 2008b Sensitivity to reward loss as an indicator of animal emotion and welfare. Biology Letters 4: 330–333. http://dx.doi.org/10.1098/rsbl.2008.0113CrossRefGoogle Scholar
Burman, OHP, Parker, RMA, Paul, ES and Mendl, MT 2009 Anxiety-induced cognitive bias in non-human animals. Physiology & Behavior 98: 345–350. http://dx.doi.org/10.1016/j.physbeh.2009.06.012CrossRefGoogle ScholarPubMed
Dawkins, MS 1990 From an animal's point of view: motivation, fitness, and animal welfare. Behavioral and Brain Sciences 13: 1–61. http://dx.doi.org/10.1017/S0140525X00077104CrossRefGoogle Scholar
Doyle, RE, Fisher, AD, Hinch, GN, Boissy, A and Lee, C 2010a Release from restraint generates a positive judgement bias in sheep. Applied Animal Behaviour Science 122: 28–34. http://dx.doi.org/10.1016/j.applanim.2009.11.003Google Scholar
Doyle, RE, Hinch, GN, Fisher, AD, Boissy, A, Henshall, JM and Lee, C 2011 Administration of serotonin inhibitor p-Chlorophenylalanine induces pessimistic-like judgement bias in sheep. Psychoneuroendocrinology 36: 279–288. http://dx.doi.org/10.1016/j.psyneuen.2010.07.018CrossRefGoogle ScholarPubMed
Doyle, RE, Vidal, S, Hinch, GN, Fisher, AD, Boissy, A and Lee, C 2010b The effect of repeated testing on judgement biases in sheep. Behavioural Processes 8: 349–352. http://dx.doi.org/10.1016/j.beproc.2010.01.019CrossRefGoogle Scholar
Enkel, T, Gholizadeh, D, von Bohlen und Halbach, O, Sanchis-Segura, C, Hurlemann, R, Spanagel, R, Gass, P and Vollmayr, B 2009 Ambiguous-cue interpretation is biased under stress- and depression-like states in rats. Neuropsychopharmacology 35: 1008–1015CrossRefGoogle ScholarPubMed
Eysenck, MW, Mogg, K, May, J, Richards, A and Mathews, A 1991 Bias in interpretation of ambiguous sentences related to threat in anxiety. Journal of Abnormal Psychology 100: 144–150. http://dx.doi.org/10.1037/0021-843X.100.2.1.44CrossRefGoogle ScholarPubMed
Eysenck, MW, Payne, S and Santos, R 2006 Anxiety and depression: past, present, and future events. Cognition & Emotion 20: 274–294. http://dx.doi.org/10.1080/02699930500220066CrossRefGoogle Scholar
Garner, M, Mogg, K and Bradley, BP 2006 Fear-relevant selective associations and social anxiety: absence of a positive bias. Behaviour Research and Therapy 44: 201–217. http://dx.doi.org/10.1016/j.brat.2004.12.007CrossRefGoogle ScholarPubMed
Gray, JA 1971 The Psychology of Fear and Stress. World University Library: London, UKGoogle Scholar
Harding, EJ, Paul, ES and Mendl, M 2004 Animal behaviour, cognitive bias and affective state. Nature 427: 312–312. http://dx.doi.org/10.1038/427312aCrossRefGoogle ScholarPubMed
Heistermann, M, Palme, R and Ganswindt, A 2006 Comparison of different enzyme immunoassays for assessment of adrenocortical activity in primates based on fecal analysis. American Journal of Primatology 68: 257–273. http://dx.doi.org/10.1002/ajp.20222CrossRefGoogle ScholarPubMed
Honess, PE and Marin, CM 2006a Behavioural and physiological aspects of stress and aggression in nonhuman primates. Neuroscience and Biobehavioral Reviews 30: 390–412. http://dx.doi.org/10.1016/j.neubiorev.2005.04.003CrossRefGoogle ScholarPubMed
Honess, PE and Marin, CM 2006b Enrichment and aggression in primates. Neuroscience and Biobehavioral Reviews 30: 413–436. http://dx.doi.org/10.1016/j.neubiorev.2005.05.002CrossRefGoogle ScholarPubMed
Jansson, B and Najström, M 2009 Is pre-attentive bias predictive of autonomic reactivity in response to a stressor? Journal of Anxiety Disorders 23: 374–380. http://dx.doi.org/10.1016/j.janxdis.2008.12.001CrossRefGoogle Scholar
MacLeod, AK and Byrne, A 1996 Anxiety, depression, and the anticipation of future positive and negative experiences. Journal of Abnormal Psychology 105: 286–289. http://dx.doi.org/10.1037/0021-843X.105.2.286CrossRefGoogle ScholarPubMed
Maestripieri, D 2000 Measuring temperament in rhesus macaques: consistency and change in emotionality over time. Behavioural Processes 49: 167–171. http://dx.doi.org/10.1016/S0376-6357(00)00083-8CrossRefGoogle ScholarPubMed
Mason, GJ and Veasey, JS 2010 How should the psychological well-being of zoo elephants be objectively investigated? Zoo Biology 29: 237–255CrossRefGoogle ScholarPubMed
Matheson, SM, Asher, L and Bateson, M 2008 Larger, enriched cages are associated with ‘optimistic’ response biases in captive European starlings (Sturnus vulgaris). Applied Animal Behaviour Science 109: 374–383CrossRefGoogle Scholar
Mathews, A and MacLeod, C 2002 Induced processing biases have causal effects on anxiety. Cognition and Emotion 16: 331–354. http://dx.doi.org/10.1080/02699930143000518CrossRefGoogle Scholar
Mendl, M 1999 Performing under pressure: stress and cognitive function. Applied Animal Behaviour Science 65: 221–244. http://dx.doi.org/10.1016/S0168-1591(99)00088-XCrossRefGoogle Scholar
Mendl, M and Paul, ES 2004 Consciousness, emotion and animal welfare: insights from cognitive science. Animal Welfare 13: S17–S25Google Scholar
Mendl, M, Burman, OHP, Parker, RMA and Paul, ES 2009 Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Applied Animal Behaviour Science 118: 161–181. http://dx.doi.org/10.1016/j.applanim.2009.02.023CrossRefGoogle Scholar
Mendl, M, Burman, OHP and Paul, ES 2010a An integrative and functional framework for the study of animal emotion and mood. Proceedings of the Royal Society B-Biological Sciences 277: 2895–2904. http://dx.doi.org/10.1098/rspb.2010.0303CrossRefGoogle Scholar
Mendl, M, Brooks, J, Basse, C, Burman, OHP, Paul, ES, Blackwell, E and Casey, R 2010b Dogs showing separation-related behavior exhibit a ‘pessimistic’ cognitive bias. Current Biology 20: R839–840. http://dx.doi.org/10.1016/j.cub.2010.08.030CrossRefGoogle ScholarPubMed
Miranda, R and Mennin, DS 2007 Depression, generalized anxiety disorder, and certainty in pessimistic predictions about the future. Cognitive Therapy and Research 31: 71–82. http://dx.doi.org/10.1007/s10608-006-9063-4CrossRefGoogle Scholar
Mogg, K, Bradley, BP, Millar, N and White, J 1995 A follow-up study of cognitive bias in generalized anxiety disorder. Behaviour Research and Therapy 33: 927–935. http://dx.doi.org/10.1016/0005-7967(95)00031-RCrossRefGoogle ScholarPubMed
Moran, MD 2003 Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100: 403–405. http://dx.doi.org/10.1034/j.1600-0706.2003.12010.xCrossRefGoogle Scholar
Nakagawa, S 2004 A farewell to Bonferroni: the problems of low statistical power and publication bias. Behavioral Ecology 15: 1044–1045. http://dx.doi.org/10.1093/beheco/arh107CrossRefGoogle Scholar
NC3Rs 2011 Non-human Primate Welfare. The National Centre for the Replacement, Refinement and Reduction of Animals in Research: London, UK. Available at: www.nc3rs.org.ukGoogle Scholar
Novak, M 2003 Self-injurious behavior in rhesus monkeys: new insights into its etiology, physiology and treatment. American Journal of Primatology 59: 3–19. http://dx.doi.org/10.1002/ajp.10063CrossRefGoogle ScholarPubMed
Ozment, JM and Lester, D 2001 Helplessness, locus of control and psychological health. The Journal of Social Psychology 141: 137–138. http://dx.doi.org/10.1080/00224540109600535CrossRefGoogle ScholarPubMed
Paul, ES, Harding, EJ and Mendl, M 2005 Measuring emotional processes in animals: the utility of a cognitive approach. Neuroscience and Biobehavioral Reviews 29: 469–491. http://dx.doi.org/10.1016/j.neubiorev.2005.01.002CrossRefGoogle ScholarPubMed
Pompilio, L, Kacelnik, A and Behmer, ST 2006 State-dependent learned valuation drives choice in an invertebrate. Science 311: 1613–1615. http://dx.doi.org/10.1126/science.1123924CrossRefGoogle Scholar
Pury, CLS 2002 Information-processing predictors of emotional response to stress. Cognition & Emotion 16: 667–683. http://dx.doi.org/10.1080/02699930143000400CrossRefGoogle Scholar
Rennie, AE and Buchanan-Smith, HM 2006a Refinement of the use of non-human primates in scientific research. Part I: the influence of humans. Animal Welfare 15: 203–213Google Scholar
Rennie, AE and Buchanan-Smith, HM 2006b Refinement of the use of non-human primates in scientific research. Part III: refinement of procedures. Animal Welfare 15: 239–261Google Scholar
Richards, A, French, CC, Calder, AJ, Webb, B, Fox, R and Young, AW 2002 Anxiety-related bias in the classification of emotionally ambiguous facial expressions. Emotion 2: 273–287. http://dx.doi.org/10.1037/1528-3542.2.3.273CrossRefGoogle ScholarPubMed
Rodd, ZA, Rosellini, RA, Stock, HS and Gallup, GG 1997 Learned helplessness in chickens (Gallus gallus): evidence for attentional bias. Learning and Motivation 28: 43–55. http://dx.doi.org/10.1006/lmot.1997.0952CrossRefGoogle Scholar
Ruys, JD, Mendoza, SP, Capitanio, JP and Mason, WA 2004 Behavioral and physiological adaptation to repeated chair restraint in rhesus macaques. Physiology & Behavior 82: 205–213. http://dx.doi.org/10.1016/j.physbeh.2004.02.031Google ScholarPubMed
Salmeto, AL, Hymel, KA, Carpenter, EC, Brilot, BO, Bateson, M and Sufka, KJ 2011 Cognitive bias in the chick anxiety-depression model. Brain Research 1373: 124–130. http://dx.doi.org/10.1016/j.brainres.2010.12.007CrossRefGoogle ScholarPubMed
Sanger, ME, Doyle, RE, Hinch, GN and Lee, C 2011 Sheep exhibit a positive judgement bias and stress-induced hyperthermia following shearing. Applied Animal Behaviour Science 131: 94–103. http://dx.doi.org/10.1016/j.applanim.2011.02.001CrossRefGoogle Scholar
Seligman, MEP 1991 Learned Optimism. Alfred A Knopf: New York, USAGoogle Scholar
Seligman, MEP 1994 What you can Change and What you Cannot. Alfred A Knopf: New York, USAGoogle Scholar
Tran, TB, Hertel, PT and Joorman, J 2011 Cognitive bias modification: induced interpretive biases affect memory. Emotion 11: 145–152. http://dx.doi.org/10.1037/a0021754CrossRefGoogle ScholarPubMed
van der Harst, JE, Baars, AM and Spruijt, BM 2003 Standard housed rats are more sensitive to rewards than enriched housed rats as reflected by their anticipatory behaviour. Behavioural Brain Research 142: 151–156. http://dx.doi.org/10.1016/S0166-4328(02)00403-5CrossRefGoogle ScholarPubMed
Veissier, I, Butterworth, A, Bock, B and Roe, E 2008 European approaches to ensure good animal welfare. Applied Animal Behaviour Science 113: 279–297. http://dx.doi.org/10.1016/j.applanim.2008.01.008CrossRefGoogle Scholar
Wilson, EJ, MacLeod, C, Mathews, A and Rutherford, E 2006 The causal role of interpretive bias in anxiety reactivity. Journal of Abnormal Psychology 115: 103–111. http://dx.doi.org/10.1037/0021-843X.115.1.103CrossRefGoogle ScholarPubMed
Woike, BA, Bender, M and Besner, N 2009 Implicit motivational states influence memory: Evidence for motive by state-dependent learning in personality. Journal of Research in Personality 43: 39–48. http://dx.doi. org/10.1016/j.jrp.2008.10.009CrossRefGoogle Scholar
Yiend, J, Mackintosh, B and Mathews, A 2005 Enduring consequences of experimentally induced biases in interpretation. Behaviour Research and Therapy 43: 779–797. http://dx.doi.org/10.1016/j.brat.2004.06.007Google ScholarPubMed