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

Animal Welfare

Volumn 21, Issue 2, 2012, Pages 185-195

  Bethell, E J ^a,b   Holmes, A ^b   MacLarnon, A ^b   Semple, S ^b  

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF ROEHAMPTON   (United Kingdom)

Author keywords

Animal welfare; Capture; Emotion; Enrichment; Husbandry procedures; Rhesus macaque

Indexed keywords

KETAMINE;

ANIMAL EXPERIMENT; ANIMAL HUSBANDRY; ANXIETY; ARTICLE; COGNITION; CONTROLLED STUDY; DEPRESSION; ENVIRONMENTAL ENRICHMENT; FOOD; HUMAN; INFORMATION PROCESSING; MACACA; MACACA MULATTA; MALE; NONHUMAN; PRIMATE; PSYCHOLOGICAL WELL BEING; RHESUS MONKEY; STIMULUS;

EID: 84860121743     PISSN: 09627286     EISSN: None     Source Type: Journal    
DOI: 10.7120/09627286.21.2.185     Document Type: Article

References (59)

1. 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 metaanalytic study. Psychological Bulletin 133: 1-24. http://dx.doi.org/10.1037/0033-2909.133.1.1
2. 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: 33-36
3. 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.2011.05.017
4. 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/ 17470210600890511
5. 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. 2007.02.003
6. 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-z
7. 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. 2010.05.001
8. 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.2010.09.030
9. 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. 2008.02.014
10. 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.2008.0113
11. 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.2009.06.012
12. 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/S0140525X00077104
13. 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.2009.11.003
14. 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.2010.07.018
15. 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.2010.01.019
16. 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: 1008-1015
17. 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.100.2.144
18. 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/10.1080/02699930500220066
19. 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.2004.12.007
20. Gray JA 1971 The Psychology of Fear and Stress. World University Library: London, UK Harding EJ, Paul ES and Mendl M 2004 Animal behaviour, cognitive bias and affective state. Nature 427: 312-312. http://dx.doi.org/10.1038/427312a
21. 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.20222
22. 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.2005.04.003
23. 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.2005.05.002
24. 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.2008.12.001
25. 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.105.2.286
26. 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)00083-8
27. Mason GJ and Veasey JS 2010 How should the psychological well-being of zoo elephants be objectively investigated? Zoo Biology 29: 237-255
28. 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: 374-383
29. 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. 1080/02699930143000518
30. 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-X
31. Mendl M and Paul ES 2004 Consciousness, emotion and animal welfare: insights from cognitive science. Animal Welfare 13: S17-S25
32. 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. 2009.02.023
33. 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. 2010.0303
34. Mendl M, Brooks J, Basse C, Burman OHP, Paul ES, Blackwell E and Casey R 2010b Dogs showing separationrelated behavior exhibit a 'pessimistic' cognitive bias. Current Biology 20: R839-840. http://dx.doi.org/10.1016/j.cub.2010.08.030
35. 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/s10608-006-9063-4
36. Mogg K, Bradley BP, Millar N and White J 1995 A followup 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-R
37. 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.x
38. 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/arh107
39. 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.uk
40. 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.10063
41. 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/10.1080/00224540109600535
42. 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.2005.01.002
43. 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.1123924
44. Pury CLS 2002 Information-processing predictors of emotional response to stress. Cognition & Emotion 16: 667-683. http://dx.doi.org/10.1080/ 02699930143000400
45. 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: 203-213
46. 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: 239-261
47. 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/10.1037/1528-3542.2.3.273
48. 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.1997.0952
49. 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. 02.031
50. Salmeto AL, Hymel KA, Carpenter EC, Brilot BO, Bateson M and Sufka KJ 2011 Cognitive bias in the chick anx-iety- depression model. Brain Research 1373: 124-130. http://dx.doi.org/10.1016/j.brainres.2010.12.007
51. 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. 02.001
52. Seligman MEP 1991 Learned Optimism. Alfred A Knopf: New York, USA
53. Seligman MEP 1994 What you can Change and What you Cannot. Alfred A Knopf: New York, USA
54. 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/a0021754
55. 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)00403-5
56. 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.2008.01.008
57. 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.115.1.103
58. 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.2008.10.009
59. 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.2004.06.007