FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS One / Are Eyes a Mirror of the Soul? What Eye Wrinkles Reveal abou...
PloS one2016; 11(10); e0164017; doi: 10.1371/journal.pone.0164017

Are Eyes a Mirror of the Soul? What Eye Wrinkles Reveal about a Horse’s Emotional State.

Abstract: Finding valid indicators of emotional states is one of the biggest challenges in animal welfare science. Here, we investigated in horses whether variation in the expression of eye wrinkles caused by contraction of the inner eyebrow raiser reflects emotional valence. By confronting horses with positive and negative conditions, we aimed to induce positive and negative emotional states, hypothesising that positive emotions would reduce whereas negative emotions would increase eye wrinkle expression. Sixteen horses were individually exposed in a balanced order to two positive (grooming, food anticipation) and two negative conditions (food competition, waving a plastic bag). Each condition lasted for 60 seconds and was preceded by a 60 second control phase. Throughout both phases, pictures of the eyes were taken, and for each horse four pictures per condition and phase were randomly selected. Pictures were scored in random order and by two experimenters blind to condition and phase for six outcome measures: qualitative impression, eyelid shape, markedness of the wrinkles, presence of eye white, number of wrinkles, and the angle between the line through the eyeball and the highest wrinkle. The angle decreased during grooming and increased during food competition compared to control phases, whereas the two phases did not differ during food anticipation and the plastic bag condition. No effects on the other outcome measures were detected. Taken together, we have defined a set of measures to assess eye wrinkle expression reliably, of which one measure was affected by the conditions the horses were exposed to. Variation in eye wrinkle expression might provide valuable information on horse welfare but further validation of specific measures across different conditions is needed.
Get Full Text
Publication Date: 2016-10-12 PubMed ID: 27732647PubMed Central: PMC5061373DOI: 10.1371/journal.pone.0164017Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigates if the expression of eye wrinkles in horses can be indicative of their emotional state. The researchers hypothesized that positive emotions would decrease eye wrinkle expression and negative emotions would increase it. The study did show changes in eye wrinkle expression under different conditions, reinforcing the idea that it may be a valuable indicator of horse welfare.

Research Methodology

This study involved a set of 16 horses that were individually subjected to different emotional conditions:

  • Two positive conditions: Grooming and food anticipation
  • Two negative conditions: Food competition and wavering a plastic bag

Each condition lasted 60 seconds and was preceded by a 60-second control phase. Photos of the horse’s eyes were taken during both phases.

Eye Wrinkle Evaluation

Four pictures per condition and phase were randomly selected for each horse. These pictures were then scored by two experimenters who were blind to the condition and phase. Six outcome measures were used to assess the eye wrinkle expression:

  • Qualitative impression
  • Eyelid shape
  • Markedness of the wrinkles
  • Presence of eye white
  • Number of wrinkles
  • The angle between the line through the eyeball and the highest wrinkle

Research Findings

The research found that the angle of the eye wrinkles reduced during grooming and increased during food competition, as compared to the control phases. However, there was no difference during food anticipation or exposure to the plastic bag.

Interestingly, none of the other outcome measures showed any significant changes across the different emotional states.

Conclusions and Further Research

Overall, the study suggests that eye wrinkle expression in horses may serve as a measure of animal welfare. Specifically, the research demonstrated that variation in the angle of eye wrinkles can reflect different emotional conditions.

However, the authors do caution that further validation of this specific measure is required across different conditions. Further research also needs to be conducted to understand whether the other outcome measures can provide similar insights into a horse’s emotional state.

Cite This Article

APA
Hintze S, Smith S, Patt A, Bachmann I, Würbel H. (2016). Are Eyes a Mirror of the Soul? What Eye Wrinkles Reveal about a Horse’s Emotional State. PLoS One, 11(10), e0164017. https://doi.org/10.1371/journal.pone.0164017

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 11
Issue: 10
Pages: e0164017
PII: e0164017

Researcher Affiliations

Hintze, Sara
  • Division of Animal Welfare, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
  • Agroscope, Swiss National Stud Farm, Avenches, Switzerland.
Smith, Samantha
  • Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, United Kingdom.
Patt, Antonia
  • Department of Animal and Avian Sciences, University of Maryland, College Park, Maryland, United States of America.
Bachmann, Iris
  • Agroscope, Swiss National Stud Farm, Avenches, Switzerland.
Würbel, Hanno
  • Division of Animal Welfare, Vetsuisse Faculty, University of Bern, Bern, Switzerland.

MeSH Terms

  • Animal Welfare
  • Animals
  • Emotions
  • Eye Color / physiology
  • Eyelids / physiology
  • Feeding Behavior
  • Female
  • Horses
  • Male
  • Skin Aging / physiology

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 41 references
  1. Mendl M, Burman OH, Paul ES. An integrative and functional framework for the study of animal emotion and mood.. Proc Biol Sci 2010 Oct 7;277(1696):2895-904.
    doi: 10.1098/rspb.2010.0303pmc: PMC2982018pubmed: 20685706google scholar: lookup
  2. Darwin C. The expression of the emotions in man and animals. London; 1872.
  3. Ekman P, Friesen W V. Measuring facial movement. Environ Psychol nonverbal Behav 1976;1:56–75.
    doi: 10.1007/bf01115465google scholar: lookup
  4. Morris JS, Frith CD, Perrett DI, Rowland D, Young AW, Calder AJ, Dolan RJ. A differential neural response in the human amygdala to fearful and happy facial expressions.. Nature 1996 Oct 31;383(6603):812-5.
    doi: 10.1038/383812a0pubmed: 8893004google scholar: lookup
  5. Vick SJ, Waller BM, Parr LA, Smith Pasqualini MC, Bard KA. A Cross-species Comparison of Facial Morphology and Movement in Humans and Chimpanzees Using the Facial Action Coding System (FACS).. J Nonverbal Behav 2007 Mar;31(1):1-20.
    doi: 10.1007/s10919-006-0017-zpmc: PMC3008553pubmed: 21188285google scholar: lookup
  6. Keating SC, Thomas AA, Flecknell PA, Leach MC. Evaluation of EMLA cream for preventing pain during tattooing of rabbits: changes in physiological, behavioural and facial expression responses.. PLoS One 2012;7(9):e44437.
    doi: 10.1371/journal.pone.0044437pmc: PMC3436883pubmed: 22970216google scholar: lookup
  7. Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, Glick S, Ingrao J, Klassen-Ross T, Lacroix-Fralish ML, Matsumiya L, Sorge RE, Sotocinal SG, Tabaka JM, Wong D, van den Maagdenberg AM, Ferrari MD, Craig KD, Mogil JS. Coding of facial expressions of pain in the laboratory mouse.. Nat Methods 2010 Jun;7(6):447-9.
    doi: 10.1038/nmeth.1455pubmed: 20453868google scholar: lookup
  8. Ahola Kohut S, Pillai Riddell R. Does the Neonatal Facial Coding System differentiate between infants experiencing pain-related and non-pain-related distress?. J Pain 2009 Feb;10(2):214-20.
    doi: 10.1016/j.jpain.2008.08.010pubmed: 19081306google scholar: lookup
  9. Cohn JF, Kruez TS, Matthews I, Yang Y, Nguyen MH, Padilla MT. Detecting depression from facial actions and vocal prosody. Affective Computing and Intelligent Interaction 2009; p. 1–7.
  10. Caeiro CC, Waller BM, Zimmermann E, Burrows AM, Davila-Ross Marina. OrangFACS: A muscle-based facial movement coding system for Oragnutans (Pongo spp). Int J Primatol 2013;34(115–129).
    doi: 10.1007/s10764-012-9652-xgoogle scholar: lookup
  11. Waller BM, Peirce K, Caeiro CC, Scheider L, Burrows AM, McCune S, Kaminski J. Paedomorphic facial expressions give dogs a selective advantage.. PLoS One 2013;8(12):e82686.
    doi: 10.1371/journal.pone.0082686pmc: PMC3873274pubmed: 24386109google scholar: lookup
  12. Wathan J, Burrows AM, Waller BM, McComb K. EquiFACS: The Equine Facial Action Coding System.. PLoS One 2015;10(8):e0131738.
    pmc: PMC4526551pubmed: 26244573doi: 10.1371/journal.pone.0131738google scholar: lookup
  13. Sotocinal SG, Sorge RE, Zaloum A, Tuttle AH, Martin LJ, Wieskopf JS, Mapplebeck JC, Wei P, Zhan S, Zhang S, McDougall JJ, King OD, Mogil JS. The Rat Grimace Scale: a partially automated method for quantifying pain in the laboratory rat via facial expressions.. Mol Pain 2011 Jul 29;7:55.
    doi: 10.1186/1744-8069-7-55pmc: PMC3163602pubmed: 21801409google scholar: lookup
  14. Holden E, Calvo G, Collins M, Bell A, Reid J, Scott EM, Nolan AM. Evaluation of facial expression in acute pain in cats.. J Small Anim Pract 2014 Dec;55(12):615-21.
    doi: 10.1111/jsap.12283pubmed: 25354833google scholar: lookup
  15. McLennan KM, Rebelo CJB, Corke MJ, Holmes M a., Leach MC, Constantino-Casas F. Development of a facial expression scale using footrot and mastitis as models of pain in sheep. Appl Anim Behav Sci 2016;176:19–26.
    doi: 10.1016/j.applanim.2016.01.007google scholar: lookup
  16. Dalla Costa E, Minero M, Lebelt D, Stucke D, Canali E, Leach MC. Development of the Horse Grimace Scale (HGS) as a pain assessment tool in horses undergoing routine castration.. PLoS One 2014;9(3):e92281.
    doi: 10.1371/journal.pone.0092281pmc: PMC3960217pubmed: 24647606google scholar: lookup
  17. Gleerup KB, Forkman B, Lindegaard C, Andersen PH. An equine pain face.. Vet Anaesth Analg 2015 Jan;42(1):103-14.
    pmc: PMC4312484pubmed: 25082060doi: 10.1111/vaa.12212google scholar: lookup
  18. Arellano D, Perales FJ, Varona J. Mood and Its Mapping onto Facial Expressions. Proc 8th Int Conf AMDO 2014;31–40.
  19. Swiss Federal Council. Animal Welfare Ordinance. 2011 p. 20.
  20. Feh C, de Mazières J. Grooming at a preferred site reduces heart rate in horses. Anim Behav 46(6):1191–4.
    doi: 10.1006/anbe.1993.1309google scholar: lookup
  21. McBride SD, Hemmings A, Robinson K. A preliminary study on the effect of massage to reduce stress in the horse. J Equine Vet Sci 2004;24(2):76–81.
    doi: 10.1016/j.jevs.2004.01.014google scholar: lookup
  22. Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J, Bakken M, Veissier I, Aubert A. Assessment of positive emotions in animals to improve their welfare.. Physiol Behav 2007 Oct 22;92(3):375-97.
    doi: 10.1016/j.physbeh.2007.02.003pubmed: 17428510google scholar: lookup
  23. Bos Rv, Meijer MK, van Renselaar JP, van der Harst JE, Spruijt BM. Anticipation is differently expressed in rats (Rattus norvegicus) and domestic cats (Felis silvestris catus) in the same Pavlovian conditioning paradigm.. Behav Brain Res 2003 Apr 17;141(1):83-9.
    doi: 10.1016/s0166-4328(02)00318-2pubmed: 12672562google scholar: lookup
  24. Bachmann I, Bernasconi P, Herrmann R, Weishaupt M a., Staﾬher M. Behavioural and physiological responses to an acute stressor in crib-biting and control horses. Appl Anim Behav Sci 2003;82(4):297–311.
    doi: 10.1016/s0168-1591(03)00086-8google scholar: lookup
  25. Ninomiya S, Kusunose R, Sato S, Terada M, Sugawara K. Effects of feeding methods on eating frustration in stabled horses. Anim Sci J 2004;75(5):465–9.
    doi: 10.1111/j.1740-0929.2004.00214.xgoogle scholar: lookup
  26. Christensen JW, Malmkvist J, Nielsen BL, Keeling LJ. Effects of a calm companion on fear reactions in naive test horses.. Equine Vet J 2008 Jan;40(1):46-50.
    doi: 10.2746/042516408X245171pubmed: 18083659google scholar: lookup
  27. Von Borstel UUK, Duncan IJH, Lundin MC, Keeling LJ. Fear reactions in trained and untrained horses from dressage and show-jumping breeding lines. Appl Anim Behav Sci 2010;125(3–4):124–31.
    doi: 10.1016/j.applanim.2010.04.015google scholar: lookup
  28. Landis JR, Koch GG. The measurement of observer agreement for categorical data.. Biometrics 1977 Mar;33(1):159-74.
    doi: 10.2307/2529310pubmed: 843571google scholar: lookup
  29. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability.. Psychol Bull 1979 Mar;86(2):420-8.
    doi: 10.1037//0033-2909.86.2.420pubmed: 18839484google scholar: lookup
  30. Landers R. Computing (ICC) as Intraclass Estimates Correlations of Interrater Reliability in SPSS. The Winnower 2015;(2:e143518.81744 (2015)):1–4.
  31. Cicchetti D V. Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. Psychol Assess 1994;6(4):284–90.
    doi: 10.1037//1040-3590.6.4.284google scholar: lookup
  32. Bates D, Maechler M, Bolker B, Walker S. lme4: Linear mixed-effects models using Eigen and S4. 2014.
  33. Christensen RHB. ordinal—Regression models for ordinal data. 2015.
  34. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC. nlme: Linear and nonlinear mixed effects models. 2015.
  35. Sandem AI, Braastad BO, Bùe KE. Eye white may indicate emotional state on a frustration-contentedness axis in dairy cows. 2002;79:1–10.
    doi: 10.1016/s0168-1591(02)00029-1google scholar: lookup
  36. Moe RO, Nordgreen J, Janczak AM, Spruijt BM, Zanella AJ, Bakken M. Trace classical conditioning as an approach to the study of reward-related behaviour in laying hens: A methodological study. Appl Anim Behav Sci 2009;121:171–8.
    doi: 10.1016/j.applanim.2009.10.002google scholar: lookup
  37. Wieland K. What are my horse’s eyes telling me?. 2013.
  38. Crowe J. Body language 101—Part two: the eyes and nose. 2009.
  39. Boissy A. Fear and fearfulness in animals.. Q Rev Biol 1995 Jun;70(2):165-91.
    doi: 10.1086/418981pubmed: 7610234google scholar: lookup
  40. De Boyer Des Roches A, Richard-Yris MA, Henry S, Ezzaouïa M, Hausberger M. Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects' emotional value.. Physiol Behav 2008 Jun 9;94(3):487-90.
    doi: 10.1016/j.physbeh.2008.03.002pubmed: 18455205google scholar: lookup
  41. Farmer K, Krueger K, Byrne RW. Visual laterality in the domestic horse (Equus caballus) interacting with humans.. Anim Cogn 2010 Mar;13(2):229-38.
    doi: 10.1007/s10071-009-0260-xpubmed: 19618222google scholar: lookup

Citations

This article has been cited 20 times.
  1. Kim SM, Cho GJ. Analysis of Various Facial Expressions of Horses as a Welfare Indicator Using Deep Learning.. Vet Sci 2023 Apr 10;10(4).
    doi: 10.3390/vetsci10040283pubmed: 37104439google scholar: lookup
  2. Kumar P, Abubakar AA, Ahmed MA, Hayat MN, Ajat M, Kaka U, Goh YM, Sazili AQ. Electroencephalogram and Physiological Responses as Affected by Slaughter Empathy in Goats.. Animals (Basel) 2023 Mar 20;13(6).
    doi: 10.3390/ani13061100pubmed: 36978640google scholar: lookup
  3. Kapteijn CM, Frippiat T, van Beckhoven C, van Lith HA, Endenburg N, Vermetten E, Rodenburg TB. Measuring heart rate variability using a heart rate monitor in horses (Equus caballus) during groundwork.. Front Vet Sci 2022;9:939534.
    doi: 10.3389/fvets.2022.939534pubmed: 36483490google scholar: lookup
  4. Neethirajan S. The Use of Artificial Intelligence in Assessing Affective States in Livestock.. Front Vet Sci 2021;8:715261.
    doi: 10.3389/fvets.2021.715261pubmed: 34409091google scholar: lookup
  5. Bremhorst A, Mills DS, Würbel H, Riemer S. Evaluating the accuracy of facial expressions as emotion indicators across contexts in dogs.. Anim Cogn 2022 Feb;25(1):121-136.
    doi: 10.1007/s10071-021-01532-1pubmed: 34338869google scholar: lookup
  6. Hintze S, Schanz L. Using the Judgment Bias Task to Identify Behavioral Indicators of Affective State: Do Eye Wrinkles in Horses Reflect Mood?. Front Vet Sci 2021;8:676888.
    doi: 10.3389/fvets.2021.676888pubmed: 34307525google scholar: lookup
  7. Lundblad J, Rashid M, Rhodin M, Haubro Andersen P. Effect of transportation and social isolation on facial expressions of healthy horses.. PLoS One 2021;16(6):e0241532.
    doi: 10.1371/journal.pone.0241532pubmed: 34086704google scholar: lookup
  8. Neethirajan S, Reimert I, Kemp B. Measuring Farm Animal Emotions-Sensor-Based Approaches.. Sensors (Basel) 2021 Jan 14;21(2).
    doi: 10.3390/s21020553pubmed: 33466737google scholar: lookup
  9. Maskato Y, Dugdale AHA, Singer ER, Kelmer G, Sutton GA. Prospective Feasibility and Revalidation of the Equine Acute Abdominal Pain Scale (EAAPS) in Clinical Cases of Colic in Horses.. Animals (Basel) 2020 Nov 29;10(12).
    doi: 10.3390/ani10122242pubmed: 33260428google scholar: lookup
  10. Rashid M, Silventoinen A, Gleerup KB, Andersen PH. Equine Facial Action Coding System for determination of pain-related facial responses in videos of horses.. PLoS One 2020;15(11):e0231608.
    doi: 10.1371/journal.pone.0231608pubmed: 33141852google scholar: lookup
  11. Lansade L, Colson V, Parias C, Reigner F, Bertin A, Calandreau L. Human Face Recognition in Horses: Data in Favor of a Holistic Process.. Front Psychol 2020;11:575808.
    doi: 10.3389/fpsyg.2020.575808pubmed: 33041946google scholar: lookup
  12. Humphrey T, Proops L, Forman J, Spooner R, McComb K. The role of cat eye narrowing movements in cat-human communication.. Sci Rep 2020 Oct 5;10(1):16503.
    doi: 10.1038/s41598-020-73426-0pubmed: 33020542google scholar: lookup
  13. Bremhorst A, Sutter NA, Würbel H, Mills DS, Riemer S. Differences in facial expressions during positive anticipation and frustration in dogs awaiting a reward.. Sci Rep 2019 Dec 17;9(1):19312.
    doi: 10.1038/s41598-019-55714-6pubmed: 31848389google scholar: lookup
  14. Bell C, Rogers S, Taylor J, Busby D. Improving the Recognition of Equine Affective States.. Animals (Basel) 2019 Dec 11;9(12).
    doi: 10.3390/ani9121124pubmed: 31835886google scholar: lookup
  15. Merkies K, Ready C, Farkas L, Hodder A. Eye Blink Rates and Eyelid Twitches as a Non-Invasive Measure of Stress in the Domestic Horse.. Animals (Basel) 2019 Aug 15;9(8).
    doi: 10.3390/ani9080562pubmed: 31443315google scholar: lookup
  16. Baciadonna L, Briefer EF, Favaro L, McElligott AG. Goats distinguish between positive and negative emotion-linked vocalisations.. Front Zool 2019;16:25.
    doi: 10.1186/s12983-019-0323-zpubmed: 31320917google scholar: lookup
  17. Schanz L, Krueger K, Hintze S. Sex and Age Don't Matter, but Breed Type Does-Factors Influencing Eye Wrinkle Expression in Horses.. Front Vet Sci 2019;6:154.
    doi: 10.3389/fvets.2019.00154pubmed: 31192235google scholar: lookup
  18. Lansade L, Nowak R, Lainé AL, Leterrier C, Bonneau C, Parias C, Bertin A. Facial expression and oxytocin as possible markers of positive emotions in horses.. Sci Rep 2018 Oct 2;8(1):14680.
    doi: 10.1038/s41598-018-32993-zpubmed: 30279565google scholar: lookup
  19. Briefer EF. Vocal contagion of emotions in non-human animals.. Proc Biol Sci 2018 Feb 28;285(1873).
    doi: 10.1098/rspb.2017.2783pubmed: 29491174google scholar: lookup
  20. Caeiro C, Guo K, Mills D. Dogs and humans respond to emotionally competent stimuli by producing different facial actions.. Sci Rep 2017 Nov 14;7(1):15525.
    doi: 10.1038/s41598-017-15091-4pubmed: 29138393google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.