Visual attention, an indicator of human-animal relationships? A study of domestic horses (Equus caballus)

Frontiers in Psychology

Volumn 5, Issue FEB, 2014, Pages

  Rochais, C ^a   Henry, S ^a   Sankey, C ^a   Nassur, F ^b   Goracka Bruzda A ^c   Hausberger, M ^a,b  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c INSTITUTE OF GENETICS AND ANIMAL BREEDING   (Poland)

Author keywords

Attentional processes; Horses; Human animal relationships; Reinforcement; Training

Indexed keywords

EID: 84897586667     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2014.00108     Document Type: Article

References (83)

1. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour 49, 227-266. doi: 10.1163/156853974X00534.
2. Anderson, J. R. (1998). Social stimuli and social rewards in primate learning and cognition. Behav. Process. 42, 159-175. doi: 10.1016/S0376-6357(97)00074-0.
3. Armony, J. L., and Dolan, R. J. (2002). Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study. Neuropsychologia 40, 817-826. doi: 10.1016/S0028-3932(01)00178-6.
4. Baragli, P., Gazzano, A., Marteli, F., and Sighieri, C. (2009). How do horses appraise humans' actions? A brief note over a practical way to assess stimulus. J. Equine Vet. Sci. 29, 739-742. doi: 10.1016/j.jevs.2009.08.006.
5. Baragli, P., Mariti, C., Petri, L., De Giorgio, F., and Sighieri, C. (2011). Does attention make the difference? Horses' response to human stimulus after 2 different training strategies. J. Vet. Behav. Clin. Appl. Res. 6, 31-38. doi: 10.1016/j.jveb.2010.08.020.
6. Basile, M., Boivin, S., Boutin, A., Blois-Heulin, C., Hausberger, M., and Lemasson, A. (2009). Socially dependent auditory laterality in domestic horses (Equus caballus). Anim. Cogn. 12, 611-619. doi: 10.1007/s10071-009-0220-5.
7. Behrmann, M., Geng, J. J., and Shomstein, S. (2004). Parietal cortex and attention. Curr. Opin. Neurobiol. 14, 212-217. doi: 10.1016/j.conb.2004.03.012.
8. Bertin, A., Hausberger, M., Henry, L., and Richard-Yris, M.-A. (2007). Adult and peer influences on starling song development. Dev. Psychobiol. 49, 362-374. doi: 10.1002/dev.20223.
9. Blois-Heulin, C. (1999). Variability in social visual attention in the red-capped mangabey (Cercocebus torquatus torquatus) and the grey-cheeked mangabey (Cercocebus albigena albigena). Folia Primatol. 70, 264-268. doi: 10.1159/000021705.
10. Boyd, L., Carbonaro, D., and Houpt, K. (1988). The 24-hour time-budget of Przewalski horses. Appl. Anim. Behav. Sci. 21, 5-17. doi: 10.1016/0168-1591(88)90098-6.
11. Call, J., Bräuer, J., Kaminski, J., and Tomasello, M. (2003). Domestic dogs (Canis familiaris) are sensitive to the attentional state of humans. J. Comp. Psychol. 117, 257-263. doi: 10.1037/0735-7036.117.3.257.
12. Chance, M. R. A., and Jolly, C. (1970). Social Groups of Monkeys, Apes and Men. London: Jonathan Cape.
13. Chance, P. (1992). The rewards of learning. Phi Delta Kappan 73, 200-207.
14. Cousillas, H., George, I., Henry, L., Richard, J.-P., and Hausberger, M. (2008). Linking social and vocal brains: could social segregation prevent a proper development of a central auditory area in a female songbird? PLoS ONE 3:e2194. doi: 10.1371/journal.pone.0002194.
15. Cousillas, H., George, I., Mathelier, M., Richard, J.-P., Henry, L., and Hausberger, M. (2006). Social experience influences the development of a central auditory area. Naturwissenschaften 93, 588-596. doi: 10.1007/s00114-006-0148-4.
16. Davids, E., Zhang, K., Tarazi, F. I., and Baldessarini, R. J. (2003). Animal models of attention-deficit hyperactivity disorder. Brain Res. Rev. 42, 1-21. doi: 10.1016/S0165-0173(02)00274-6.
17. Emery, N. J. (2000). The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci. Biobehav. Rev. 24, 581-604. doi: 10.1016/S0149-7634(00)00025-7.
18. Feh, C. (2005). "Relationship and communication in socially natural horse herds," in The Domestic Horse, eds D. Mills and S. McDonnell (Cambridge: Cambridge University Press), 83-93.
19. Feh, C., and De Mazières, J. (1993). Grooming at a preferred site reduces heart rate in horses. Anim. Behav. 46, 1191-1194. doi: 10.1006/anbe.1993.1309.
20. Fureix, C., Jego, P., Sankey, C., and Hausberger, M. (2009). How horses (Equus caballus) see the world: humans as significant "objects". Anim. Cogn. 12, 643-654. doi: 10.1007/s10071-009-0223-2.
21. Giurfa, M. (2013). Cognition with few neurons: higher-order learning in insects. Trends Neurosci. 36, 285-294. doi: 10.1016/j.tins.2012.12.011.
22. Hattori, Y., Kuroshima, H., and Fujita, K. (2007). I know you are not looking at me: capuchin monkeys' (Cebus apella) sensitivity to human attentional states. Anim. Cogn. 10, 141-148. doi: 10.1007/s10071-006-0049-0.
23. Hausberger, M., and Muller, C. (2002). A brief note on some possible factors involved in the reactions of horses to humans. Appl. Anim. Behav. Sci. 76, 339-344. doi: 10.1016/S0168-1591(02)00016-3.
24. Hausberger, M., Roche, H., Henry, S., and Visser, E. K. (2008). A review of the human-horse relationship. Appl. Anim. Behav. Sci. 109, 1-24. doi: 10.1016/j.applanim.2007.04.015.
25. Henry, S., Hemery, D., Richard, M.-A., and Hausberger, M. (2005). Human-mare relationships and behaviour of foals toward humans. Appl. Anim. Behav. Sci. 93, 341-362. doi: 10.1016/j.applanim.2005.01.008.
26. Henry, S., Richard-Yris, M.-A., and Hausberger, M. (2006). Influence of various early human-foal interferences on subsequent human-foal relationship. Dev. Psychobiol. 48, 712-718. doi: 10.1002/dev.20189.
27. Henry, S., Richard-Yris, M.-A., Tordjman, S., and Hausberger, M. (2009). Neonatal handling affects durably bonding and social development. PLoS ONE 4:e5216. doi: 10.1371/journal.pone.0005216.
28. Hinde, R. A. (1979). Towards Understanding Relationships. London: Academic Press.
29. Horn, L., Virányi, Z., Miklósi, Á., Huber, L., and Range, F. (2012). Domestic dogs (Canis familiaris) flexibly adjust their human-directed behavior to the actions of their human partners in a problem situation. Anim. Cogn. 15, 57-71. doi: 10.1007/s10071-011-0432-3.
30. Jezierski, T., Jaworski, Z., and Górecka, A. (1999). Effects of handling on behaviour and heart rate in Konik horses: comparison of stable and forest reared youngstock. Appl. Anim. Behav. Sci. 62, 1-11. doi: 10.1016/S0168-1591(98)00209-3.
31. Kaminski, J., Call, J., and Tomasello, M. (2004). Body orientation and face orientation: two factors controlling apes' begging behavior from humans. Anim. Cogn. 7, 216-223. doi: 10.1007/s10071-004-0214-2.
32. Keeling, L. J., Jonare, L., and Lanneborn, L. (2009). Investigating horse-human interactions: the effect of a nervous human. Vet. J. 181, 70-71. doi: 10.1016/j.tvjl.2009.03.013.
33. Kirkden, R. D., and Pajor, E. A. (2006). Using preference, motivation and aversion tests to ask scientific questions about animals' feelings. Appl. Anim. Behav. Sci. 100, 29-47. doi: 10.1016/j.applanim.2006.04.009.
34. Knight, R. T., Grabowecky, M. F., and Scabini, D. (1995). Role of human prefrontal cortex in attention control. Adv. Neurol. 66, 21-34. discussion: 34-36.
35. Krapp, A. (1999). Interest, motivation and learning: an educational-psychological perspective. Eur. J. Psychol. Educ. 14, 23-40. doi: 10.1007/BF03173109.
36. Krueger, K., Flauger, B., Farmer, K., and Maros, K. (2011). Horses (Equus caballus) use human local enhancement cues and adjust to human attention. Anim. Cogn. 14, 187-201. doi: 10.1007/s10071-010-0352-7.
37. Kruschke, J. K. (2003). Attention in Learning. Curr. Dir. Psychol. Sci. 12, 171-175. doi: 10.1111/1467-8721.01254.
38. Lampe, J., and Andre, J. (2012). Cross-modal recognition of human individuals in domestic horses (Equus caballus). Anim. Cogn. 15, 623-630. doi: 10.1007/s10071-012-0490-1.
39. Lemasson, A., Boutin, A., Boivin, S., Blois-Heulin, C., and Hausberger, M. (2009). Horse (Equus caballus) whinnies: a source of social information. Anim. Cogn. 12, 693-704. doi: 10.1007/s10071-009-0229-9.
40. Lesimple, C., Sankey, C., Richard, M. A., and Hausberger, M. (2012). Do horses expect humans to solve their problems? Front. Psychol. 3:306. doi: 10.3389/fpsyg.2012.00306.
41. Libera, C. D., and Chelazzi, L. (2006). Visual selective attention and the effects of monetary rewards. Psychol. Sci. 17, 222-227. doi: 10.1111/j.1467-9280.2006.01689.x.
42. Maille, A., Engelhart, L., Bourjade, M., and Blois-Heulin, C. (2012). To beg, or not to beg? that is the question: mangabeys modify their production of requesting gestures in response to human's attentional states. PLoS ONE 7:e41197. doi: 10.1371/journal.pone.0041197.
43. Marler, P. (1965). "Communication in monkeys and apes," in Primate Behavior, ed I. DeVore (New York, NY: Holt, Rinehart and Winston), 544-584.
44. Maros, K., Gácsi, M., and Miklósi, Á. (2008). Comprehension of human pointing gestures in horses (Equus caballus). Anim. Cogn. 11, 457-466. doi: 10.1007/s10071-008-0136-5.
45. Maxime, H. (2013). RVAideMemoire: Diverse Basic Statistical and Graphical Functions. R Package Version 0.9-27. Available online at: http://CRAN.R-project.org/package=RVAideMemoire.
46. McDonnell, S. M. (2000). How to rehabilitate horses with injection shyness (or any procedure non-compliance). AEEP Proc. 46, 168-172.
47. McGreevy, P. D., and McLean, A. N. (2011). Equitation Science. John Wiley & Sons.
48. McKinley, J., and Sambrook, T. D. (2000). Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus). Anim. Cogn. 3, 13-22. doi: 10.1007/s100710050046.
49. Micheletta, J., and Waller, B. M. (2012). Friendship affects gaze following in a tolerant species of macaque, Macaca nigra. Anim. Behav. 83, 459-467. doi: 10.1016/j.anbehav.2011.11.018.
50. Miklósi, Á., and Soproni, K. (2006). A comparative analysis of animals' understanding of the human pointing gesture. Anim. Cogn. 9, 81-93. doi: 10.1007/s10071-005-0008-1.
51. Mills, D. S., and McDonnell, S. M. (2005). The Domestic Horse: The Origins, Development and Management of its Behaviour. Cambridge: Cambridge University Press.
52. Nebel, K., Wiese, H., Stude, P., de Greiff, A., Diener, H.-C., and Keidel, M. (2005). On the neural basis of focused and divided attention. Cogn. Brain Res. 25, 760-776. doi: 10.1016/j.cogbrainres.2005.09.011.
53. Oades, R. D., and Sartory, G. (1997). The problems of inattention: methods and interpretations. Behav. Brain Res. 88, 3-10. doi: 10.1016/S0166-4328(97)02303-6.
54. Posner, M. I., Cohen, Y., and Rafal, R. D. (1982). Neural systems control of spatial orienting. Philos. Trans. R. Soc. Lond. B Biol. Sci. 298, 187-198. doi: 10.1098/rstb.1982.0081.
55. Posner, M. I., Snyder, C. R., and Davidson, B. J. (1980). Attention and the detection of signals. J. Exp. Psychol. Gen. 109, 160-174. doi: 10.1037/0096-3445.109.2.160.
56. Proops, L., and McComb, K. (2010). Attributing attention: the use of human-given cues by domestic horses (Equus caballus). Anim. Cogn. 13, 197-205. doi: 10.1007/s10071-009-0257-5.
57. Proops, L., and McComb, K. (2012). Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans. Proc. R. Soc. B Biol. Sci. 279, 3131-3138. doi: 10.1098/rspb.2012.0626.
58. Proops, L., McComb, K., and Reby, D. (2009). Cross-modal individual recognition in domestic horses (Equus caballus). Proc. Natl. Acad. Sci. U.S.A. 106, 947-951. doi: 10.1073/pnas.0809127105.
59. Quay, H. C. (1997). Inhibition and attention deficit hyperactivity disorder. J. Abnorm. Child Psychol. 25, 7-13. doi: 10.1023/A:1025799122529.
60. Range, F., Horn, L., Bugnyar, T., Gajdon, G. K., and Huber, L. (2009). Social attention in keas, dogs, and human children. Anim. Cogn. 12, 181-192. doi: 10.1007/s10071-008-0181-0.
61. Range, F., and Huber, L. (2007). Attention in common marmosets: implications for social-learning experiments. Anim. Behav. 73, 1033-1041. doi: 10.1016/j.anbehav.2006.07.015.
62. Raymond, J. (2009). "Interactions of attention, emotion and motivation," in Progress in Brain Research, ed N. Srinivasan (New York, NY: Elsevier), 293-308.
63. R Development Core Team. (2011). R: A Language And Environment For Statistical Computing. Vienna: R Foundation for Statistical Computing. Available online at: http://www. R-project.org/.
64. Sankey, C., Henry, S., André, N., Richard-Yris, M.-A., and Hausberger, M. (2011). Do horses have a concept of person? PLoS ONE 6:e18331. doi: 10.1371/journal.pone.0018331.
65. Sankey, C., Henry, S., Górecka-Bruzda, A., Richard-Yris, M.-A., and Hausberger, M. (2010c). The way to a man's heart is through his stomach: what about horses? PLoS ONE 5:e15446. doi: 10.1371/journal.pone.0015446.
66. Sankey, C., Richard-Yris, M.-A., Leroy, H., Henry, S., and Hausberger, M. (2010a). Positive interactions lead to lasting positive memories in horses, Equus caballus. Anim. Behav. 79, 869-875. doi: 10.1016/j.anbehav.2009.12.037.
67. Sankey, C., Richard-Yris, M.-A., Henry, S., Fureix, C., Nassur, F., and Hausberger, M. (2010b). Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Anim. Cogn. 13, 753-764. doi: 10.1007/s10071-010-0326-9.
68. Schultz, W. (2004). Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology. Curr. Opin. Neurobiol. 14, 139-147. doi: 10.1016/j.conb.2004.03.017.
69. Schwab, C., and Huber, L. (2006). Obey or not obey? Dogs (Canis familiaris) behave differently in response to attentional states of their owners. J. Comp. Psychol. 120, 169-175. doi: 10.1037/0735-7036.120.3.169.
70. Siegel, S., and Castellan, N. (1988). Non Parametric Statistics for the Behavioral Sciences, 2nd Edn. Boston, MA: McGraw-Hill. 399.
71. Spaethe, J., Tautz, J., and Chittka, L. (2006). Do honeybees detect colour targets using serial or parallel visual search? J. Exp. Biol. 209, 987-993. doi: 10.1242/jeb.02124.
72. Stormark, K. M., and Hugdahl, K. (1997). Conditioned emotional cueing of spatial attentional shifts in a go/no-go RT task. Int. J. Psychophysiol. 27, 241-248. doi: 10.1016/S0167-8760(97)00065-2.
73. Taylor, J. G., and Fragopanagos, N. F. (2005). The interaction of attention and emotion. Neural Netw. 18, 353-369. doi: 10.1016/j.neunet.2005.03.005.
74. Toates, F. (1986). Motivational Systems. Cambridge: Cambridge University Press.
75. Topál, J., Miklósi, A., and Csányi, V. (1997). Dog-human relationship affects problem-solving behavior in the dog. Anthrozoos 10, 214-224. doi: 10.2752/089279397787000987.
76. Treisman, A. M. (1969). Strategies and models of selective attention. Psychol. Rev. 76, 282-299. doi: 10.1037/h0027242.
77. van Swinderen, B., and Greenspan, R. J. (2003). Salience modulates 20-30 Hz brain activity in Drosophila. Nat. Neurosci. 6, 579-586. doi: 10.1038/nn1054.
78. von Borstel, U. U., Heatly Duncan, I. J., Shoveller, A. K., Merkies, K., Keeling, L. J., and Millman, S. T. (2009). Impact of riding in a coercively obtained Rollkur posture on welfare and fear of performance horses. Appl. Anim. Behav. Sci. 116, 228-236. doi: 10.1016/j.applanim.2008.10.001.
79. Waiblinger, S., Boivin, X., Pedersen, V., Tosi, M.-V., Janczak, A. M., Visser, E. K., et al. (2006). Assessing the human-animal relationship in farmed species: a critical review. Appl. Anim. Behav. Sci. 101, 185-242. doi: 10.1016/j.applanim.2006.02.001.
80. Waring, G. (2003). Horse Behavior, 2nd Edn. Norwich, NY: Noyes Publications/William Andrew Publishing. 442.
81. Weigel, R. M. (1979). The facial expression of the brown capuchin monkey (Cebus apella). Behavior 68, 250-276. doi: 10.1163/156853979X00331.
82. Xitco, M. J., Gory, J. D., and Ii, S. A. K. (2004). Dolphin pointing is linked to the attentional behavior of a receiver. Anim. Cogn. 7, 231-238. doi: 10.1007/s10071-004-0217-z.
83. Xitco, M. J., Gory, J. D., and Kuczaj, S. A. (2001). Spontaneous pointing by bottlenose dolphins (Tursiops truncatus). Anim. Cogn. 4, 115-123. doi: 10.1007/s100710100107.