Measuring affect-related cognitive bias: Do mice in opposite affective states react differently to negative and positive stimuli?


Autoři: Anna C. Trevarthen aff001;  Sarah Kappel aff002;  Claire Roberts aff001;  Emily M. Finnegan aff001;  Elizabeth S. Paul aff001;  Isaac Planas-Sitjà aff003;  Michael T. Mendl aff001;  Carole Fureix aff002
Působiště autorů: Bristol Veterinary School, University of Bristol, Bristol, United Kingdom aff001;  School of Biological & Marine Science, University of Plymouth, Plymouth, Devon, United Kingdom aff002;  Department of Biological Sciences, Graduate School of Science and Engineering, Tokyo Metropolitan University, Tokyo, Japan aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226438

Souhrn

Affect-driven cognitive biases can be used as an indicator of affective (emotional) state. Since humans in negative affective states demonstrate greater responses to negatively-valenced stimuli, we investigated putative affect-related bias in mice by monitoring their response to unexpected, task-irrelevant stimuli of different valence. Thirty-one C57BL/6J and 31 DBA/2J females were individually trained to return to their home-cage in a runway. Mice then underwent an affective manipulation acutely inducing a negative (NegAff) or a comparatively less negative (CompLessNeg) affective state before immediately being tested in the runway with either an ‘attractive’ (familiar food) or ‘threatening’ (flashing light) stimulus. Mice were subsequently trained and tested again (same affective manipulation) with the alternative stimulus. As predicted, mice were slower to approach the light and spent more time with the food. DBA/2J mice were slower than C57BL/6J overall. Contrary to predictions, NegAff mice tended to approach both stimuli more readily than CompLessNeg mice, especially the light, and even more so for DBA/2Js. Although the stimuli successfully differentiated the response of mice to unexpected, task-irrelevant stimuli, further refinement may be required to disentangle the effects of affect manipulation and arousal on the response to valenced stimuli. The results also highlight the significant importance of considering strain differences when developing cognitive tasks.

Klíčová slova:

Animal behavior – Animal cognition – Animal welfare – Attention – Behavior – Emotions – Food consumption – Mice


Zdroje

1. Paul ES, Harding EJ, Mendl M. Measuring emotional processes in animals: the utility of a cognitive approach. Neurosci Biobehav Rev. 2005;29: 469–491. doi: 10.1016/j.neubiorev.2005.01.002 15820551

2. Boly M, Seth AK, Wilke M, Ingmundson P, Baars B, Laureys S, et al. Consciousness in humans and non-human animals: recent advances and future directions. Front Psychol. 2013;4: 625. doi: 10.3389/fpsyg.2013.00625 24198791

3. Eysenck MW, Derakshan N, Santos R, Calvo MG. Anxiety and cognitive performance: Attentional control theory. Emotion. 2007;7: 336–353 17516812

4. MacLeod KA, Byrne A. Anxiety, depression, and the anticipation of future positive and negative experience. J Abnorm Psychol. 1993;102: 238–247.

5. Mathews A, MacLeod C. Cognitive Vulnerability to Emotional Disorders. Annu Rev Clin Psychol. 2005;1: 167–195. doi: 10.1146/annurev.clinpsy.1.102803.143916 17716086

6. Eysenck MW, Byrne A. Anxiety and susceptibility to distraction. Pers Individ Dif. 1992;13: 793–798. doi: 10.1016/0191-8869(92)90052-Q

7. Mineka S, Watson D, Clark LA. COMORBIDITY OF ANXIETY AND UNIPOLAR MOOD DISORDERS. Annu Rev Psychol. 1998;49: 377–412. doi: 10.1146/annurev.psych.49.1.377 9496627

8. Mathews A, MacLeod C. Cognitive Approaches to Emotion and Emotional Disorders. Annu Rev Psychol. 1994;45: 25–50. doi: 10.1146/annurev.ps.45.020194.000325 8135504

9. Bradley BP, Mogg K, Williams R. Implicit and explicit memory for emotional information in non-clinical subjects. Behav Res Ther. 1994;32: 65–78. doi: 10.1016/0005-7967(94)90085-x 8135724

10. MacLeod C, McLaughlin K. Implicit and explicit memory bias in anxiety: a conceptual replication. Behav Res Ther. 1995;33: 1–14. Available: http://www.ncbi.nlm.nih.gov/pubmed/7872931 doi: 10.1016/0005-7967(94)e0004-3

11. Harding EJ, Paul ES, Mendl M. Cognitive bias and affective state. Nature. 2004;427: 312–312. doi: 10.1038/427312a 14737158

12. Mendl M, Burman OHP, Parker RMA, Paul ES. Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying mechanisms. Appl Anim Behav Sci. 2009;118: 161–181. doi: 10.1016/J.APPLANIM.2009.02.023

13. Baciadonna L, McElligott A. The use of judgement bias to assess welfare in farm livestock. Anim Welf. 2015;24: 81–91. doi: 10.7120/09627286.24.1.081

14. Gygax L. The A to Z of statistics for testing cognitive judgement bias. Anim Behav. 2014;95: 59–69. doi: 10.1016/J.ANBEHAV.2014.06.013

15. Bethell EJ. A “How-To” Guide for Designing Judgment Bias Studies to Assess Captive Animal Welfare. J Appl Anim Welf Sci. 2015;18: S18–S42. doi: 10.1080/10888705.2015.1075833 26440495

16. Hales CA, Stuart SA, Anderson MH, Robinson ESJ. Modelling cognitive affective biases in major depressive disorder using rodents. Br J Pharmacol. 2014;171: 4524–4538. doi: 10.1111/bph.12603 24467454

17. Burman OHP, Parker R, Paul ES, Mendl M. A spatial judgement task to determine background emotional state in laboratory rats, Rattus norvegicus. Anim Behav. 2008;76: 801–809. doi: 10.1016/j.anbehav.2008.02.014

18. Bateson M, Nettle D. Development of a cognitive bias methodology for measuring low mood in chimpanzees. PeerJ. 2015;3: e998. doi: 10.7717/peerj.998 26082875

19. Pomerantz O, Terkel J, Suomi SJ, Paukner A. Stereotypic head twirls, but not pacing, are related to a ‘pessimistic’-like judgment bias among captive tufted capuchins (Cebus apella). Anim Cogn. 2012;15: 689–698. doi: 10.1007/s10071-012-0497-7 22526692

20. Deakin A, Browne WJ, Hodge JJL, Paul ES, Mendl M. A Screen-Peck Task for Investigating Cognitive Bias in Laying Hens. Weary D, editor. PLoS One. 2016;11: e0158222. doi: 10.1371/journal.pone.0158222 27410229

21. Bateson M, Emmerson M, Ergün G, Monaghan P, Nettle D. Opposite Effects of Early-Life Competition and Developmental Telomere Attrition on Cognitive Biases in Juvenile European Starlings. Carere C, editor. PLoS One. 2015;10: e0132602. doi: 10.1371/journal.pone.0132602 26222390

22. Mendl M, Paul ES, Chittka L. Animal Behaviour: Emotion in Invertebrates? Curr Biol. 2011;21: R463–R465. doi: 10.1016/j.cub.2011.05.028 21683898

23. Paul E, Mendl M. Animal sentience an interdisciplinary journal on animal feeling [Internet]. Animal Sentience. Humane Society Institute for Science and Policy; 2016. https://animalstudiesrepository.org/animsent/vol1/iss9/16

24. Bateson M, Desire S, Gartside SE, Wright GA. Agitated Honeybees Exhibit Pessimistic Cognitive Biases. Curr Biol. 2011;21: 1070–1073. doi: 10.1016/j.cub.2011.05.017 21636277

25. Perry CJ, Baciadonna L, Chittka L. Unexpected rewards induce dopamine-dependent positive emotion-like state changes in bumblebees. Science. 2016;353: 1529–1531. doi: 10.1126/science.aaf4454 27708101

26. d’Ettorre P, Carere C, Demora L, Le Quinquis P, Signorotti L, Bovet D. Individual differences in exploratory activity relate to cognitive judgement bias in carpenter ants. Behav Processes. 2017;134: 63–69. doi: 10.1016/j.beproc.2016.09.008 27688007

27. Deakin A, Mendl M, Browne WJ, Paul ES, Hodge JJL. State-dependent judgement bias in Drosophila: evidence for evolutionarily primitive affective processes. Biol Lett. 2018;14: 20170779. doi: 10.1098/rsbl.2017.0779 29491031

28. Monk JE, Doyle RE, Colditz IG, Belson S, Cronin GM, Lee C. Towards a more practical attention bias test to assess affective state in sheep. Kret ME, editor. PLoS One. 2018;13: e0190404. doi: 10.1371/journal.pone.0190404 29293636

29. Boleij H, van’t Klooster J, Lavrijsen M, Kirchhoff S, Arndt SS, Ohl F. A test to identify judgement bias in mice. Behav Brain Res. 2012;233: 45–54. doi: 10.1016/j.bbr.2012.04.039 22562041

30. Hintze S, Melotti L, Colosio S, Bailoo JD, Boada-Saña M, Würbel H, et al. A cross-species judgement bias task: integrating active trial initiation into a spatial Go/No-go task. Sci Rep. 2018;8: 5104. doi: 10.1038/s41598-018-23459-3 29572529

31. Matheson SM, Asher L, Bateson M. Larger, enriched cages are associated with ‘optimistic’ response biases in captive European starlings (Sturnus vulgaris). Appl Anim Behav Sci. 2008;109: 374–383. doi: 10.1016/J.APPLANIM.2007.03.007

32. Parker RMA, Paul ES, Burman OHP, Browne WJ, Mendl M. Housing conditions affect rat responses to two types of ambiguity in a reward-reward discrimination cognitive bias task. Behav Brain Res. 2014;274: 73–83. doi: 10.1016/j.bbr.2014.07.048 25106739

33. Brydges NM, Hall L. A shortened protocol for assessing cognitive bias in rats. J Neurosci Methods. 2017;286: 1–5. doi: 10.1016/j.jneumeth.2017.05.015 28502553

34. Salmeto AL, Hymel KA, Carpenter EC, Brilot BO, Bateson M, Sufka KJ. Cognitive bias in the chick anxiety–depression model. Brain Res. 2011;1373: 124–130. doi: 10.1016/j.brainres.2010.12.007 21156165

35. Jones S, Neville V, Higgs L, Paul ES, Dayan P, Robinson ESJ, et al. Assessing animal affect: an automated and self-initiated judgement bias task based on natural investigative behaviour. Sci Rep. 2018;8: 12400. doi: 10.1038/s41598-018-30571-x 30120315

36. Mogg K, Bradley BP. A cognitive-motivational analysis of anxiety. Behav Res Ther. 1998;36: 809–48. Available: http://www.ncbi.nlm.nih.gov/pubmed/9701859 doi: 10.1016/s0005-7967(98)00063-1

37. Cisler JM, Koster EHW. Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. Clin Psychol Rev. 2010;30: 203–216. doi: 10.1016/j.cpr.2009.11.003 20005616

38. Barry TJ, Vervliet B, Hermans D. An integrative review of attention biases and their contribution to treatment for anxiety disorders. Front Psychol. 2015;6: 968. doi: 10.3389/fpsyg.2015.00968 26217284

39. Brilot BO, Bateson M. Water bathing alters threat perception in starlings. Biol Lett. 2012;8: 379–81. doi: 10.1098/rsbl.2011.1200 22250131

40. Brilot BO, Asher L, Bateson M. Water bathing alters the speed–accuracy trade-off of escape flights in European starlings. Anim Behav. 2009;78: 801–807. doi: 10.1016/J.ANBEHAV.2009.07.022

41. Cussen VA, Mench JA. Personality predicts cognitive bias in captive psittacines, Amazona amazonica. Anim Behav. 2014;89: 123–130. doi: 10.1016/j.anbehav.2013.12.022

42. Lee C, Verbeek E, Doyle R, Bateson M. Attention bias to threat indicates anxiety differences in sheep. Biol Lett. 2016;12: 20150977. doi: 10.1098/rsbl.2015.0977 27277950

43. Lee C, Cafe LM, Robinson SL, Doyle RE, Lea JM, Small AH, et al. Anxiety influences attention bias but not flight speed and crush score in beef cattle. Appl Anim Behav Sci. 2018;205: 210–215. doi: 10.1016/J.APPLANIM.2017.11.003

44. Bethell EJ, Holmes A, MacLarnon A, Semple S. Evidence That Emotion Mediates Social Attention in Rhesus Macaques. Vitzthum VJ, editor. PLoS One. 2012;7: e44387. doi: 10.1371/journal.pone.0044387 22952968

45. Bar-Haim Y, Lamy D, Pergamin L, Bakermans-Kranenburg MJ, van IJzendoorn MH. Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychol Bull. 2007;133: 1–24. doi: 10.1037/0033-2909.133.1.1 17201568

46. Mogg K, Bradley BP. Anxiety and attention to threat: Cognitive mechanisms and treatment with attention bias modification. Behav Res Ther. 2016;87: 76–108. doi: 10.1016/j.brat.2016.08.001 27616718

47. Bradley BP, Mogg K, Falla SJ, Hamilton LR. Attentional Bias for Threatening Facial Expressions in Anxiety: Manipulation of Stimulus Duration. Cogn Emot. 1998;12: 737–753. doi: 10.1080/026999398379411

48. Williams JM, Mathews A, MacLeod C. The emotional Stroop task and psychopathology. Psychol Bull. 1996;120: 3–24. Available: http://www.ncbi.nlm.nih.gov/pubmed/8711015 doi: 10.1037/0033-2909.120.1.3

49. Lapointe M-LB, Blanchette I, Duclos M, Langlois F, Provencher MD, Tremblay S. Attentional bias, distractibility and short-term memory in anxiety. Anxiety, Stress Coping. 2013;26: 293–313. doi: 10.1080/10615806.2012.687722 22762442

50. Matthews G, Jones DM, Chamberlain AG. Refining the measurement of mood: The UWIST Mood Adjective Checklist. Br J Psychol. 1990;81: 17–42. doi: 10.1111/j.2044-8295.1990.tb02343.x

51. Carver CS, Scheier MF, Segerstrom SC. Optimism. Clin Psychol Rev. 2010;30: 879–889. doi: 10.1016/j.cpr.2010.01.006 20170998

52. Kress L, Bristle M, Aue T. Seeing through rose-colored glasses: How optimistic expectancies guide visual attention. de Fockert J, editor. PLoS One. 2018;13: e0193311. doi: 10.1371/journal.pone.0193311 29466420

53. Segerstrom SC. Optimism and Attentional Bias for Negative and Positive Stimuli. Personal Soc Psychol Bull. 2001;27: 1334–1343. doi: 10.1177/01461672012710009

54. Li X, He S, Zhou Z, Wang Z. ERP Studies on Attention Bias of Optimistic Individuals towards Social Information. NeuroQuantology. 2018;16. doi: 10.14704/nq.2018.16.5.1307

55. Crump A, Arnott G, Bethell EJ. Affect-Driven Attention Biases as Animal Welfare Indicators: Review and Methods. Anim an open access J from MDPI. 2018;8. doi: 10.3390/ani8080136 30087230

56. Kloke V, Schreiber RS, Bodden C, Möllers J, Ruhmann H, Kaiser S, et al. Hope for the Best or Prepare for the Worst? Towards a Spatial Cognitive Bias Test for Mice. Skoulakis EMC, editor. PLoS One. 2014;9: e105431. doi: 10.1371/journal.pone.0105431 25137069

57. Vandamme TF. Use of rodents as models of human diseases. J Pharm Bioallied Sci. 2014;6: 2–9. doi: 10.4103/0975-7406.124301 24459397

58. Johnson M. Laboratory Mice and Rats. Mater Methods. 2012;2. doi: 10.13070/mm.en.2.113

59. Tilly S-LC, Dallaire J, Mason GJ. Middle-aged mice with enrichment-resistant stereotypic behaviour show reduced motivation for enrichment. Anim Behav. 2010;80: 363–373. doi: 10.1016/J.ANBEHAV.2010.06.008

60. Fureix C, Walker M, Harper L, Reynolds K, Saldivia-Woo A, Mason G. Stereotypic behaviour in standard non-enriched cages is an alternative to depression-like responses in C57BL/6 mice. Behav Brain Res. 2016;305: 186–190. doi: 10.1016/j.bbr.2016.02.005 26876137

61. Cabib S. The neurobiology of stereotypy II: the role of stress. Stereotypic animal behaviour: fundamentals and applications to welfare. Wallingford: CABI; pp. 227–255.

62. Wolfer DP, Litvin O, Morf S, Nitsch RM, Lipp H-P, Würbel H. Laboratory animal welfare: Cage enrichment and mouse behaviour. Nature. 2004;432: 821–822. doi: 10.1038/432821a 15602544

63. Waddell J, Dunnett C, Falls WA. C57BL/6J and DBA/2J mice differ in extinction and renewal of extinguished conditioned fear. Behav Brain Res. 2004;154: 567–576. doi: 10.1016/j.bbr.2004.03.025 15313046

64. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, et al. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl). 1997;132: 107–124. doi: 10.1007/s002130050327 9266608

65. Altemus M, Sarvaiya N, Neill Epperson C. Sex differences in anxiety and depression clinical perspectives. Front Neuroendocrinol. 2014;35: 320–30. doi: 10.1016/j.yfrne.2014.05.004 24887405

66. Walker M, Fureix C, Palme R, Mason G. Co-housing rodents with different coat colours as a simple, non-invasive means of individual identification: validating mixed-strain housing for C57BL/6 and DBA/2 mice. PLoS One. 2013;8: e77541. doi: 10.1371/journal.pone.0077541 24204864

67. Blizard DA, Weinheimer VK, Klein LC, Petrill SA, Cohen R, McClearn GE. “Return to home cage” as a reward for maze learning in young and old genetically heterogeneous mice. Comp Med. 2006;56: 196–201. Available: http://www.ncbi.nlm.nih.gov/pubmed/16774128

68. Hurst JL, West RS. Taming anxiety in laboratory mice. Nat Methods. 2010;7: 825–826. doi: 10.1038/nmeth.1500 20835246

69. Gouveia K, Hurst JL. Reducing Mouse Anxiety during Handling: Effect of Experience with Handling Tunnels. Mintz EM, editor. PLoS One. 2013;8: e66401. doi: 10.1371/journal.pone.0066401 23840458

70. Monleon S, Parra A, Simon VM, Brain PF, D’Aquila P, Willner P. Attenuation of sucrose consumption in mice by chronic mild stress and its restoration by imipramine. Psychopharmacology (Berl). 1995;117: 453–457. doi: 10.1007/BF02246218 7604147

71. Archer J. Tests for emotionality in rats and mice: A review. Anim Behav. 1973;21: 205–235. doi: 10.1016/s0003-3472(73)80065-x 4578750

72. Guillot P-V, Chapouthier G. Intermale aggression and dark/light preference in ten inbred mouse strains. Behav Brain Res. 1996;77: 211–213. doi: 10.1016/0166-4328(95)00163-8 8762172

73. Baron SP, Meltzer LT. Mouse strains differ under a simple schedule of operant learning. Behav Brain Res. 2001;118: 143–52. Available: http://www.ncbi.nlm.nih.gov/pubmed/11164511 doi: 10.1016/s0166-4328(00)00322-3

74. Gouveia K, Hurst JL. Optimising reliability of mouse performance in behavioural testing: the major role of non-aversive handling. Sci Rep. 2017;7: 44999. doi: 10.1038/srep44999 28322308

75. Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015;67: 1–48. doi: 10.18637/jss.v067.i01

76. Biss RK, Hasher L. Delighted and distracted: Positive affect increases priming for irrelevant information. Emotion. 2011;11: 1474–1478. doi: 10.1037/a0023855 21707151

77. Fredrickson BL. The broaden-and-build theory of positive emotions. Philos Trans R Soc Lond B Biol Sci. 2004;359: 1367–78. doi: 10.1098/rstb.2004.1512 15347528

78. Novak J, Bailoo JD, Melotti L, Rommen J, Würbel H. An exploration based cognitive bias test for mice: Effects of handling method and stereotypic behaviour. PLoS One. 2015; doi: 10.1371/journal.pone.0130718 26154309

79. Clarkson JM, Dwyer DM, Flecknell PA, Leach MC, Rowe C. Handling method alters the hedonic value of reward in laboratory mice. Sci Rep. 2018;8: 2448. doi: 10.1038/s41598-018-20716-3 29402923

80. Bradley BP, Mogg K, Millar N, Bonham-Carter C, Fergusson E, Jenkins J, et al. Attentional Biases for Emotional Faces. Cogn Emot. 1997;11: 25–42. doi: 10.1080/026999397380014

81. Sanger ME, Doyle RE, Hinch GN, Lee C. Sheep exhibit a positive judgement bias and stress-induced hyperthermia following shearing. Appl Anim Behav Sci. 2011;131: 94–103. doi: 10.1016/J.APPLANIM.2011.02.001

82. Ferguson M, Rebrin I, Forster MJ, Sohal RS. Comparison of metabolic rate and oxidative stress between two different strains of mice with varying response to caloric restriction. Exp Gerontol. 2008;43: 757–63. doi: 10.1016/j.exger.2008.04.016 18541398

83. Lewis SR, Ahmed S, Dym C, Khaimova E, Kest B, Bodnar RJ. Inbred mouse strain survey of sucrose intake. Physiol Behav. 2005;85: 546–556. doi: 10.1016/j.physbeh.2005.06.003 15996693

84. Lewis SR, Dym C, Chai C, Singh A, Kest B, Bodnar RJ. Genetic variance contributes to ingestive processes: A survey of eleven inbred mouse strains for fat (Intralipid) intake. Physiol Behav. 2007;90: 82–94. doi: 10.1016/j.physbeh.2006.08.028 17028044

85. Atalayer D, Rowland NE. Comparison of C57BL/6 and DBA/2 mice in food motivation and satiety. Physiol Behav. 2010;99: 679–683. doi: 10.1016/j.physbeh.2010.02.001 20138902

86. MacLeod C, Mathews A, Tata P. Attentional bias in emotional disorders. J Abnorm Psychol. 1986;95: 15–20. Available: http://www.ncbi.nlm.nih.gov/pubmed/3700842 doi: 10.1037//0021-843x.95.1.15

87. Kret ME, Jaasma L, Bionda T, Wijnen JG. Bonobos (Pan paniscus) show an attentional bias toward conspecifics’ emotions. Proc Natl Acad Sci U S A. 2016;113: 3761–6. doi: 10.1073/pnas.1522060113 26976586

88. Wilson DA, Tomonaga M. Exploring attentional bias towards threatening faces in chimpanzees using the dot probe task. Chao L, editor. PLoS One. 2018;13: e0207378. doi: 10.1371/journal.pone.0207378 30485317

89. van Rooijen R, Ploeger A, Kret ME. The dot-probe task to measure emotional attention: A suitable measure in comparative studies? Psychon Bull Rev. 2017;24: 1686–1717. doi: 10.3758/s13423-016-1224-1 28092078


Článek vyšel v časopise

PLOS One


2019 Číslo 12