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Animals : an open access journal from MDPI2021; 11(6); 1643; doi: 10.3390/ani11061643

Towards Machine Recognition of Facial Expressions of Pain in Horses.

Abstract: Automated recognition of human facial expressions of pain and emotions is to a certain degree a solved problem, using approaches based on computer vision and machine learning. However, the application of such methods to horses has proven difficult. Major barriers are the lack of sufficiently large, annotated databases for horses and difficulties in obtaining correct classifications of pain because horses are non-verbal. This review describes our work to overcome these barriers, using two different approaches. One involves the use of a manual, but relatively objective, classification system for facial activity (Facial Action Coding System), where data are analyzed for pain expressions after coding using machine learning principles. We have devised tools that can aid manual labeling by identifying the faces and facial keypoints of horses. This approach provides promising results in the automated recognition of facial action units from images. The second approach, recurrent neural network end-to-end learning, requires less extraction of features and representations from the video but instead depends on large volumes of video data with ground truth. Our preliminary results suggest clearly that dynamics are important for pain recognition and show that combinations of recurrent neural networks can classify experimental pain in a small number of horses better than human raters.
Publication Date: 2021-06-01 PubMed ID: 34206077PubMed Central: PMC8229776DOI: 10.3390/ani11061643Google Scholar: Lookup
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  • Journal Article
  • Review

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 focuses on recognizing pain expressions in horses using machine learning principles and computer vision. The study devises tools for manual labeling, and explores the use of recurrent neural networks for a complete, end-to-end learning process.

Objective and Challenges

  • The research attempts to automate the recognition of facial expressions of pain in horses. Currently, automatic detection of human facial expressions is manageable due to advances in computer vision and machine learning, but this hasn’t been adequately applied to horses.
  • There are two main obstacles to this study: the lack of a large and annotated database for horse expressions, and difficulties in correctly identifying pain in horses given their inability to verbally communicate.

Pain Recognition Approach

  • The researchers employed two main methods to tackle the issue. The first one involved the use of the Facial Action Coding System (FACS), a manual yet relatively objective classification system for facial activities. After using this system to encode data, the researchers applied machine learning principles to analyze the data for pain expressions.
  • They created tools that assist with manual labeling. These tools can identify horse faces and facial features, providing a significant breakthrough towards the automatic recognition of facial action units from images.

Learning Process with Recurrent Neural Networks

  • The second method relied on recurrent neural network end-to-end learning, which requires less extraction of features and representations from videos. Instead, it depends heavily on a large amount of video data with ground truth.
  • The preliminary results of the study indicate that dynamics are crucial for recognizing pain. Furthermore, the use of recurrent neural networks for classification outperformed human raters when detecting experimental pain in horses.

Concluding Remarks

  • Though this study was preliminarily successful in automating the process of recognizing pain expressions in horses, it emphasizes the need for further research, specifically in compiling a comprehensive, annotated database of horse facial expressions.

Cite This Article

APA
Andersen PH, Broomé S, Rashid M, Lundblad J, Ask K, Li Z, Hernlund E, Rhodin M, Kjellström H. (2021). Towards Machine Recognition of Facial Expressions of Pain in Horses. Animals (Basel), 11(6), 1643. https://doi.org/10.3390/ani11061643

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 11
Issue: 6
PII: 1643

Researcher Affiliations

Andersen, Pia Haubro
  • Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, SE 75007 Uppsala, Sweden.
Broomé, Sofia
  • Division of Robotics, Perception and Learning, KTH Royal Institute of Technology, SE 100044 Stockholm, Sweden.
Rashid, Maheen
  • Department of Computer Science, University of California at Davis, California, CA 95616, USA.
Lundblad, Johan
  • Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, SE 75007 Uppsala, Sweden.
Ask, Katrina
  • Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, SE 75007 Uppsala, Sweden.
Li, Zhenghong
  • Division of Robotics, Perception and Learning, KTH Royal Institute of Technology, SE 100044 Stockholm, Sweden.
  • Department of Computer Science, Stony Brook University, New York, NY 11794, USA.
Hernlund, Elin
  • Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, SE 75007 Uppsala, Sweden.
Rhodin, Marie
  • Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, SE 75007 Uppsala, Sweden.
Kjellström, Hedvig
  • Division of Robotics, Perception and Learning, KTH Royal Institute of Technology, SE 100044 Stockholm, Sweden.

Grant Funding

  • 2020-01840 and 2016-01760 / Svenska Forskningsru00e5det Formas
  • 2016-03967 / Vetenskapsru00e5det

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 122 references
  1. Egenvall A, Penell JC, Bonnett BN, Olson P, Pringle J. Mortality of Swedish horses with complete life insurance between 1997 and 2000: variations with sex, age, breed and diagnosis.. Vet Rec 2006 Mar 25;158(12):397-406.
    doi: 10.1136/vr.158.12.397pubmed: 16565338google scholar: lookup
  2. Stover S.M.. The epidemiology of Thoroughbred racehorse injuries.. Clin. Tech. Equine Pract. 2003;2:312–322.
  3. Logan AA, Nielsen BD. Training Young Horses: The Science behind the Benefits.. Animals (Basel) 2021 Feb 9;11(2).
    doi: 10.3390/ani11020463pmc: PMC7916178pubmed: 33572461google scholar: lookup
  4. Price J, Marques JM, Welsh EM, Waran NK. Pilot epidemiological study of attitudes towards pain in horses.. Vet Rec 2002 Nov 9;151(19):570-5.
    doi: 10.1136/vr.151.19.570pubmed: 12452357google scholar: lookup
  5. Waran N, Williams VM, Clarke N, Bridge IS. Recognition of pain and use of analgesia in horses by veterinarians in New Zealand.. N Z Vet J 2010 Dec;58(6):274-80.
    doi: 10.1080/00480169.2010.69402pubmed: 21151212google scholar: lookup
  6. Bateson P.. Assessment of pain in animals.. Anim. Behav. 1991;42:827–839.
  7. Raekallio M, Heinonen KM, Kuussaari J, Vainio O. Pain alleviation in animals: attitudes and practices of Finnish veterinarians.. Vet J 2003 Mar;165(2):131-5.
    doi: 10.1016/S1090-0233(02)00186-7pubmed: 12573601google scholar: lookup
  8. Capner CA, Lascelles BD, Waterman-Pearson AE. Current British veterinary attitudes to perioperative analgesia for dogs.. Vet Rec 1999 Jul 24;145(4):95-9.
    doi: 10.1136/vr.145.4.95pubmed: 10461733google scholar: lookup
  9. Huxley JN, Whay HR. Current attitudes of cattle practitioners to pain and the use of analgesics in cattle.. Vet Rec 2006 Nov 11;159(20):662-8.
    doi: 10.1136/vr.159.20.662pubmed: 17099174google scholar: lookup
  10. Fajt VR, Wagner SA, Norby B. Analgesic drug administration and attitudes about analgesia in cattle among bovine practitioners in the United States.. J Am Vet Med Assoc 2011 Mar 15;238(6):755-67.
    doi: 10.2460/javma.238.6.755pubmed: 21401433google scholar: lookup
  11. Norring M, Wikman I, Hokkanen AH, Kujala MV, Hänninen L. Empathic veterinarians score cattle pain higher.. Vet J 2014 Apr;200(1):186-90.
    doi: 10.1016/j.tvjl.2014.02.005pubmed: 24685101google scholar: lookup
  12. Grégoire M, Coll MP, Tremblay MPB, Prkachin KM, Jackson PL. Repeated exposure to others' pain reduces vicarious pain intensity estimation.. Eur J Pain 2016 Nov;20(10):1644-1652.
    doi: 10.1002/ejp.888pubmed: 27150129google scholar: lookup
  13. Thomsen PT, Anneberg I, Herskin MS. Differences in attitudes of farmers and veterinarians towards pain in dairy cows.. Vet J 2012 Oct;194(1):94-7.
    doi: 10.1016/j.tvjl.2012.02.025pubmed: 22516921google scholar: lookup
  14. EU. Animal Welfare.. [(accessed on 23 April 2021)]; Available online: https://ec.europa.eu/food/animals/welfare_en.
  15. FVE. European Veterinary Code of Conduct.. [(accessed on 23 April 2021)];2019 Available online: fve.org/european-code-of.conduct-2019/2019.
  16. Graubner C, Gerber V, Doherr M, Spadavecchia C. Clinical application and reliability of a post abdominal surgery pain assessment scale (PASPAS) in horses.. Vet J 2011 May;188(2):178-83.
    doi: 10.1016/j.tvjl.2010.04.029pubmed: 20627635google scholar: lookup
  17. van Loon JP, Van Dierendonck MC. Monitoring acute equine visceral pain with the Equine Utrecht University Scale for Composite Pain Assessment (EQUUS-COMPASS) and the Equine Utrecht University Scale for Facial Assessment of Pain (EQUUS-FAP): A scale-construction study.. Vet J 2015 Dec;206(3):356-64.
    doi: 10.1016/j.tvjl.2015.08.023pubmed: 26526526google scholar: lookup
  18. Bussières G, Jacques C, Lainay O, Beauchamp G, Leblond A, Cadoré JL, Desmaizières LM, Cuvelliez SG, Troncy E. Development of a composite orthopaedic pain scale in horses.. Res Vet Sci 2008 Oct;85(2):294-306.
    doi: 10.1016/j.rvsc.2007.10.011pubmed: 18061637google scholar: lookup
  19. Lindegaard C, Gleerup KB, Thomsen MH, Martinussen T, Jacobsen S, Andersen PH. Anti-inflammatory effects of intra-articular administration of morphine in horses with experimentally induced synovitis.. Am J Vet Res 2010 Jan;71(1):69-75.
    doi: 10.2460/ajvr.71.1.69pubmed: 20043783google scholar: lookup
  20. Raekallio M., Taylor P.M., Bloomfield M.. A comparison of methods for evaluation of pain and distress after orthopaedic surgery in horses.. J. Vet. Anaesth. 1997;24:17–20.
  21. Price J, Catriona S, Welsh EM, Waran NK. Preliminary evaluation of a behaviour-based system for assessment of post-operative pain in horses following arthroscopic surgery.. Vet Anaesth Analg 2003 Jul;30(3):124-37.
  22. Sellon DC, Roberts MC, Blikslager AT, Ulibarri C, Papich MG. Effects of continuous rate intravenous infusion of butorphanol on physiologic and outcome variables in horses after celiotomy.. J Vet Intern Med 2004 Jul-Aug;18(4):555-63.
  23. Gleerup K.B., Lindegaard C.. Recognition and quantification of pain in horses: A tutorial review.. Equine Vet. Educ. 2016;28:47–57.
    doi: 10.1111/eve.12383google scholar: lookup
  24. Love E.J.. Assessment and management of pain in horses.. Equine Vet. Educ. 2009;21:46–48.
    doi: 10.2746/095777309X390290google scholar: lookup
  25. de Grauw JC, van Loon JP. Systematic pain assessment in horses.. Vet J 2016 Mar;209:14-22.
    doi: 10.1016/j.tvjl.2015.07.030pubmed: 26831169google scholar: lookup
  26. Williams AC. Facial expression of pain: an evolutionary account.. Behav Brain Sci 2002 Aug;25(4):439-55; discussion 455-88.
    doi: 10.1017/S0140525X02000080pubmed: 12879700google scholar: lookup
  27. Cohen Kadosh K, Johnson MH. Developing a cortex specialized for face perception.. Trends Cogn Sci 2007 Sep;11(9):367-9.
    doi: 10.1016/j.tics.2007.06.007pubmed: 17631408google scholar: lookup
  28. Deyo KS, Prkachin KM, Mercer SR. Development of sensitivity to facial expression of pain.. Pain 2004 Jan;107(1-2):16-21.
    doi: 10.1016/S0304-3959(03)00263-Xpubmed: 14715384google scholar: lookup
  29. Poole GD, Craig KD. Judgments of genuine, suppressed, and faked facial expressions of pain.. J Pers Soc Psychol 1992 Nov;63(5):797-805.
    doi: 10.1037/0022-3514.63.5.797pubmed: 1447693google scholar: lookup
  30. Matsumoto D., Hwang H.S.. Evidence for training the ability to read microexpressions of emotion.. Motiv. Emot. 2011;35:181–191.
    doi: 10.1007/s11031-011-9212-2google scholar: lookup
  31. Tate AJ, Fischer H, Leigh AE, Kendrick KM. Behavioural and neurophysiological evidence for face identity and face emotion processing in animals.. Philos Trans R Soc Lond B Biol Sci 2006 Dec 29;361(1476):2155-72.
    doi: 10.1098/rstb.2006.1937pmc: PMC1764842pubmed: 17118930google scholar: lookup
  32. Correia-Caeiro C, Guo K, Mills DS. Perception of dynamic facial expressions of emotion between dogs and humans.. Anim Cogn 2020 May;23(3):465-476.
    doi: 10.1007/s10071-020-01348-5pmc: PMC7181561pubmed: 32052285google scholar: lookup
  33. Ekman P., Friesen W., Hagar J.. Facial Action Coding System.. Research Nexus; Salt Lake City, UT, USA: 2002.
  34. Waller BM, Vick SJ, Parr LA, Bard KA, Pasqualini MC, Gothard KM, Fuglevand AJ. Intramuscular electrical stimulation of facial muscles in humans and chimpanzees: Duchenne revisited and extended.. Emotion 2006 Aug;6(3):367-82.
    doi: 10.1037/1528-3542.6.3.367pmc: PMC2826128pubmed: 16938079google scholar: lookup
  35. Sayette M.A., Cohn J.F., Wertz J.M., Perrott M.A., Parrott D.J.. A psychometric evaluation of the facial action coding system for assessing spontaneous expression.. J. Nonverbal Behav. 2001;25:167–185.
    doi: 10.1023/A:1010671109788google scholar: lookup
  36. 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
  37. Julle-Danière É, Micheletta J, Whitehouse J, Joly M, Gass C, Burrows AM, Waller BM. MaqFACS (Macaque Facial Action Coding System) can be used to document facial movements in Barbary macaques (Macaca sylvanus).. PeerJ 2015;3:e1248.
    doi: 10.7717/peerj.1248pmc: PMC4579026pubmed: 26401458google scholar: lookup
  38. Caeiro C.C., Waller B.M., Zimmermann E., Burrows A.M., Davila-Ross M.. OrangFACS: A Muscle-Based Facial Movement Coding System for Orangutans (Pongo spp.). Int. J. Primatol. 2013;34:115–129.
    doi: 10.1007/s10764-012-9652-xgoogle scholar: lookup
  39. Clark PR, Waller BM, Burrows AM, Julle-Danière E, Agil M, Engelhardt A, Micheletta J. Morphological variants of silent bared-teeth displays have different social interaction outcomes in crested macaques (Macaca nigra).. Am J Phys Anthropol 2020 Nov;173(3):411-422.
    doi: 10.1002/ajpa.24129pubmed: 32820559google scholar: lookup
  40. Correia-Caeiro C, Holmes K, Miyabe-Nishiwaki T. Extending the MaqFACS to measure facial movement in Japanese macaques (Macaca fuscata) reveals a wide repertoire potential.. PLoS One 2021;16(1):e0245117.
  41. Waller B.M., Lembeck M., Kuchenbuch P., Burrows A.M., Liebal K.. GibbonFACS: A Muscle-Based Facial Movement Coding System for Hylobatids.. Int. J. Primatol. 2012;33:809–821.
    doi: 10.1007/s10764-012-9611-6google scholar: lookup
  42. 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.
  43. Caeiro C.C., Burrows A.M., Waller B.M.. Development and application of CatFACS: Are human cat adopters influenced by cat facial expressions?. Appl. Anim. Behav. Sci. 2017;189:66–78.
  44. Wathan J, Burrows AM, Waller BM, McComb K. EquiFACS: The Equine Facial Action Coding System.. PLoS One 2015;10(8):e0131738.
  45. Burrows A., Diogo R., Waller B., Kaminski J.. Variation of Facial Musculature between Wolves and Domestic Dogs: Evolutionary Divergence in Facial Movement.. Faseb J. 2017;31:577.3.
  46. Waller BM, Parr LA, Gothard KM, Burrows AM, Fuglevand AJ. Mapping the contribution of single muscles to facial movements in the rhesus macaque.. Physiol Behav 2008 Sep 3;95(1-2):93-100.
  47. Prkachin K.M., Craig K.D.. Expressing pain: The communication and interpretation of facial pain signals.. J. Nonverbal Behav. 1995;19:191–205.
    doi: 10.1007/BF02173080google scholar: lookup
  48. Hill ML, Craig KD. Detecting deception in facial expressions of pain: accuracy and training.. Clin J Pain 2004 Nov-Dec;20(6):415-22.
  49. Lucey P., Cohn J.F., Prkachin K.M., Solomon P.E., Matthews I.. Painful data: The UNBC-McMaster shoulder pain expression archive database. Proceedings of the 2011 IEEE International Conference on Automatic Face & Gesture Recognition (FG); Santa Barbera, CA, USA. 21–25 March 2011; pp. 57–64.
    doi: 10.1109/FG.2011.5771462google scholar: lookup
  50. Rosenberg EL, Zanesco AP, King BG, Aichele SR, Jacobs TL, Bridwell DA, MacLean KA, Shaver PR, Ferrer E, Sahdra BK, Lavy S, Wallace BA, Saron CD. Intensive meditation training influences emotional responses to suffering.. Emotion 2015 Dec;15(6):775-90.
    doi: 10.1037/emo0000080pubmed: 25938614google scholar: lookup
  51. 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.
  52. 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.
  53. Miller AL, Leach MC. The Mouse Grimace Scale: A Clinically Useful Tool?. PLoS One 2015;10(9):e0136000.
  54. McLennan K.M., Miller A.L., Dalla Costa E., Stucke D., Corke M.J., Broom D.M., Leach M.C.. Conceptual and methodological issues relating to pain assessment in mammals: The development and utilisation of pain facial expression scales.. Appl. Anim. Behav. Sci. 2019;217:1–15.
  55. Dyson S, Pollard D. Application of a Ridden Horse Pain Ethogram and Its Relationship with Gait in a Convenience Sample of 60 Riding Horses.. Animals (Basel) 2020 Jun 17;10(6).
    doi: 10.3390/ani10061044pmc: PMC7341225pubmed: 32560486google scholar: lookup
  56. Dyson S., Berger J.M., Ellis A.D., Mullard J.. Can the presence of musculoskeletal pain be determined from the facial expressions of ridden horses (FEReq)?. J. Vet. Behav. Clin. Appl. Res. 2017;19:78–89.
  57. Tuyttens F.A.M., Stadig L., Heerkens J.L.T., Van laer E., Buijs S., Ampe B.. Opinion of applied ethologists on expectation bias, blinding observers and other debiasing techniques.. Appl. Anim. Behav. Sci. 2016;181:27–33.
  58. Bartlett MS, Littlewort GC, Frank MG, Lee K. Automatic decoding of facial movements reveals deceptive pain expressions.. Curr Biol 2014 Mar 31;24(7):738-43.
    doi: 10.1016/j.cub.2014.02.009pmc: PMC4034269pubmed: 24656830google scholar: lookup
  59. Littlewort G.C., Bartlett M.S., Lee K.. Faces of Pain: Automated Measurement of Spontaneous Facial Expressions of Genuine and Posed Pain. Proceedings of the ICMI’07, 9th International Conference on Multimodal Interfaces; Nagoya, Japan. 12–15 November 2007; pp. 15–21.
  60. Bartlett M.S., Littlewort G., Frank M., Lainscsek C., Fasel I., Movellan J., Soc I.C.. Fully automatic facial action recognition in spontaneous behavior. Proceedings of the Seventh International Conference on Automatic Face and Gesture Recognition; Southampton, UK. 10–12 April 2006; pp. 223–228.
  61. Bartlett M.S., Littlewort G., Frank M., Lainscsek C., Fasel I., Movellan J.. Recognizing facial expression: Machine learning and application to spontaneous behavior. Proceedings of the 2005 IEEE Computer Society Conference on Computer Vision and Pattern Recognition; San Diego, CA, USA. 20–25 June 2005; pp. 568–573.
  62. Huang J., Craig K., Diaz D., Sikka K., Ahmed A., Terrones L., Littlewort G., Goodwin M., Bartlett M.. Automated facial expression analysis can detect clinical pain in youth in the post-operative setting.. J. Pain. 2014;15:S3.
  63. Srinivasan R, Golomb JD, Martinez AM. A Neural Basis of Facial Action Recognition in Humans.. J Neurosci 2016 Apr 20;36(16):4434-42.
  64. Sikka K, Ahmed AA, Diaz D, Goodwin MS, Craig KD, Bartlett MS, Huang JS. Automated Assessment of Children's Postoperative Pain Using Computer Vision.. Pediatrics 2015 Jul;136(1):e124-31.
    doi: 10.1542/peds.2015-0029pmc: PMC4485009pubmed: 26034245google scholar: lookup
  65. Zhang X., Yin L., Cohn J., Canavan S., Reale M., Horowitz A., Liu P., Girard J.. BP4D-Spontaneous: A High-Resolution Spontaneous 3D Dynamic Facial Expression Database.. Image Vis. Comput. 2014;32:692–706.
  66. Mavadati S.M., Mahoor M.H., Bartlett K., Trinh P., Cohn J.F.. DISFA: A Spontaneous Facial Action Intensity Database.. IEEE Trans. Affect. Comput. 2013;4:151–160.
    doi: 10.1109/T-AFFC.2013.4google scholar: lookup
  67. Rolnick D., Veit A., Belongie S., Shavit N.. Deep Learning is Robust to Massive Label Noise.. arXiv 20181705.10694.
  68. Erin Browne M, Hadjistavropoulos T, Prkachin K, Ashraf A, Taati B. Pain Expressions in Dementia: Validity of Observers' Pain Judgments as a Function of Angle of Observation.. J Nonverbal Behav 2019;43(3):309-327.
    doi: 10.1007/s10919-019-00303-4pmc: PMC6656786pubmed: 31404130google scholar: lookup
  69. Sneddon L.U., Elwood R.W., Adamo S.A., Leach M.C.. Defining and assessing animal pain.. Anim. Behav. 2014;97:201–212.
  70. Seminowicz DA, Laferriere AL, Millecamps M, Yu JS, Coderre TJ, Bushnell MC. MRI structural brain changes associated with sensory and emotional function in a rat model of long-term neuropathic pain.. Neuroimage 2009 Sep;47(3):1007-14.
  71. Vila Pouca C., Brown C.. Contemporary topics in fish cognition and behaviour.. Curr. Opin. Behav. Sci. 2017;16:46–52.
  72. Descovich KA, Wathan J, Leach MC, Buchanan-Smith HM, Flecknell P, Farningham D, Vick SJ. Facial expression: An under-utilised tool for the assessment of welfare in mammals.. ALTEX 2017;34(3):409-429.
    doi: 10.14573/altex.1607161pubmed: 28214916google scholar: lookup
  73. Raja SN, Carr DB, Cohen M, Finnerup NB, Flor H, Gibson S, Keefe FJ, Mogil JS, Ringkamp M, Sluka KA, Song XJ, Stevens B, Sullivan MD, Tutelman PR, Ushida T, Vader K. The revised International Association for the Study of Pain definition of pain: concepts, challenges, and compromises.. Pain 2020 Sep 1;161(9):1976-1982.
  74. Craig KD. Social communication model of pain.. Pain 2015 Jul;156(7):1198-1199.
  75. Rutherford K.M.D.. Assessing pain in animals.. Anim. Welf. 2002;11:31–53.
  76. Ashley FH, Waterman-Pearson AE, Whay HR. Behavioural assessment of pain in horses and donkeys: application to clinical practice and future studies.. Equine Vet J 2005 Nov;37(6):565-75.
    doi: 10.2746/042516405775314826pubmed: 16295937google scholar: lookup
  77. Coles B., Birgitsdottir L., Andersen P.H.. Out of Sight but Not out of Clinician’s Mind: Using Remote Video Surveillance to Disclose Concealed Pain Behavior in Hospitalized Horses. Proceedings of the International Association for the Study of Pain 17th World Congress; Boston, MA, USA. 15–18 September 2018; p. 471121.
  78. Torcivia C, McDonnell S. In-Person Caretaker Visits Disrupt Ongoing Discomfort Behavior in Hospitalized Equine Orthopedic Surgical Patients.. Animals (Basel) 2020 Jan 27;10(2).
    doi: 10.3390/ani10020210pmc: PMC7070845pubmed: 32012670google scholar: lookup
  79. Ask K, Rhodin M, Tamminen LM, Hernlund E, Haubro Andersen P. Identification of Body Behaviors and Facial Expressions Associated with Induced Orthopedic Pain in Four Equine Pain Scales.. Animals (Basel) 2020 Nov 19;10(11).
    doi: 10.3390/ani10112155pmc: PMC7699379pubmed: 33228117google scholar: lookup
  80. Korshunov P., Ooi W.T.. Video quality for face detection, recognition, and tracking.. ACM Trans. Multimed. Comput. Commun. Appl. 2011;7:14.
    doi: 10.1145/2000486.2000488google scholar: lookup
  81. Gleerup KB, Forkman B, Lindegaard C, Andersen PH. An equine pain face.. Vet Anaesth Analg 2015 Jan;42(1):103-14.
    doi: 10.1111/vaa.12212pmc: PMC4312484pubmed: 25082060google scholar: lookup
  82. 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.
  83. Dalla Costa E, Stucke D, Dai F, Minero M, Leach MC, Lebelt D. Using the Horse Grimace Scale (HGS) to Assess Pain Associated with Acute Laminitis in Horses (Equus caballus).. Animals (Basel) 2016 Aug 3;6(8).
    doi: 10.3390/ani6080047pmc: PMC4997272pubmed: 27527224google scholar: lookup
  84. van Loon JP, Van Dierendonck MC. Monitoring equine head-related pain with the Equine Utrecht University scale for facial assessment of pain (EQUUS-FAP).. Vet J 2017 Feb;220:88-90.
    doi: 10.1016/j.tvjl.2017.01.006pubmed: 28190503google scholar: lookup
  85. 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
  86. VanDierendonck MC, van Loon JP. Monitoring acute equine visceral pain with the Equine Utrecht University Scale for Composite Pain Assessment (EQUUS-COMPASS) and the Equine Utrecht University Scale for Facial Assessment of Pain (EQUUS-FAP): A validation study.. Vet J 2016 Oct;216:175-7.
    doi: 10.1016/j.tvjl.2016.08.004pubmed: 27687948google scholar: lookup
  87. Weary D.M., Niel L., Flower F.C., Fraser D.. Identifying and preventing pain in animals.. Appl. Anim. Behav. Sci. 2006;100:64–76.
  88. Dai F, Leach M, MacRae AM, Minero M, Costa ED. Does Thirty-Minute Standardised Training Improve the Inter-Observer Reliability of the Horse Grimace Scale (HGS)? A Case Study.. Animals (Basel) 2020 Apr 30;10(5).
    doi: 10.3390/ani10050781pmc: PMC7277819pubmed: 32365927google scholar: lookup
  89. Gleerup K.B., Forkman B., Lindegaard C., Andersen P.H.. Facial expressions as a tool for pain recognition in horses. Proceedings of the 10th International Equitation Science Conference; Bredsten, Denmark. 7–9 August 2014.
  90. Guesgen M.J., Beausoleil N.J., Minot E.O., Stewart M., Jones G., Stafford K.J.. The effects of age and sex on pain sensitivity in young lambs.. Appl. Anim. Behav. Sci. 2011;135:51–56.
  91. Reijgwart ML, Schoemaker NJ, Pascuzzo R, Leach MC, Stodel M, de Nies L, Hendriksen CFM, van der Meer M, Vinke CM, van Zeeland YRA. The composition and initial evaluation of a grimace scale in ferrets after surgical implantation of a telemetry probe.. PLoS One 2017;12(11):e0187986.
  92. Ijichi C., Collins L.M., Elwood R.W.. Pain expression is linked to personality in horses.. Appl. Anim. Behav. Sci. 2014;152:38–43.
  93. Guesgen MJ, Beausoleil NJ, Stewart M. Effects of early human handling on the pain sensitivity of young lambs.. Vet Anaesth Analg 2013 Jan;40(1):55-62.
  94. Clark C, Murrell J, Fernyhough M, O'Rourke T, Mendl M. Long-term and trans-generational effects of neonatal experience on sheep behaviour.. Biol Lett 2014 Jul;10(7).
    doi: 10.1098/rsbl.2014.0273pmc: PMC4126620pubmed: 25115031google scholar: lookup
  95. Rhodin M, Egenvall A, Haubro Andersen P, Pfau T. Head and pelvic movement asymmetries at trot in riding horses in training and perceived as free from lameness by the owner.. PLoS One 2017;12(4):e0176253.
  96. Rhodin M, Persson-Sjodin E, Egenvall A, Serra Bragança FM, Pfau T, Roepstorff L, Weishaupt MA, Thomsen MH, van Weeren PR, Hernlund E. Vertical movement symmetry of the withers in horses with induced forelimb and hindlimb lameness at trot.. Equine Vet J 2018 Nov;50(6):818-824.
    doi: 10.1111/evj.12844pmc: PMC6175082pubmed: 29658147google scholar: lookup
  97. Van de Water E, Oosterlinck M, Korthagen NM, Duchateau L, Dumoulin M, van Weeren PR, Olijve J, van Doorn DA, Pille F. The lipopolysaccharide model for the experimental induction of transient lameness and synovitis in Standardbred horses.. Vet J 2021 Apr;270:105626.
    doi: 10.1016/j.tvjl.2021.105626pubmed: 33641810google scholar: lookup
  98. Lindegaard C, Frost AB, Thomsen MH, Larsen C, Hansen SH, Andersen PH. Pharmacokinetics of intra-articular morphine in horses with lipopolysaccharide-induced synovitis.. Vet Anaesth Analg 2010 Mar;37(2):186-95.
  99. Kunz M, Meixner D, Lautenbacher S. Facial muscle movements encoding pain-a systematic review.. Pain 2019 Mar;160(3):535-549.
  100. Wagner AE. Effects of stress on pain in horses and incorporating pain scales for equine practice.. Vet Clin North Am Equine Pract 2010 Dec;26(3):481-92.
    doi: 10.1016/j.cveq.2010.07.001pubmed: 21056295google scholar: lookup
  101. Trindade PHE, Hartmann E, Keeling LJ, Andersen PH, Ferraz GC, Paranhos da Costa MJR. Effect of work on body language of ranch horses in Brazil.. PLoS One 2020;15(1):e0228130.
  102. Kunz M, Lautenbacher S. The faces of pain: a cluster analysis of individual differences in facial activity patterns of pain.. Eur J Pain 2014 Jul;18(6):813-23.
  103. Rashid M., Broomé S., Andersen P.H., Gleerup K.B., Lee Y.J.. What should I annotate? An automatic tool for finding video segments for EquiFACS annotation. In Measuring Behaviour 2018 Conference Proceedings. Grant R.A., Allen T., Spink A., Sullivan M., editors. Manchester Metropolitan University; Manchester, UK: 2018. pp. 164–165.
  104. Lucey P., Cohn J.F., Kanade T., Saragih J., Ambadar Z., Matthews I.. The Extended Cohn-Kanade Dataset (CK+): A complete dataset for action unit and emotion-specified expression. Proceedings of the 2010 IEEE Computer Society Conference on Computer Vision and Pattern Recognition—Workshops; San Francisco, CA, USA. 13–18 June 2010; pp. 94–101.
  105. Littlewort G., Whitehill J., Wu T., Fasel I., Frank M., Movellan J., Bartlett M.. The computer expression recognition toolbox (CERT). Face Gesture 2011.
    doi: 10.1109/fg.2011.5771414google scholar: lookup
  106. Köstinger M., Wohlhart P., Roth P.M., Bischof H.. Annotated Facial Landmarks in the Wild: A large-scale, real-world database for facial landmark localization. Proceedings of the 2011 IEEE International Conference on Computer Vision Workshops (ICCV Workshops); Barcelona, Spain. 6–13 November 2011; pp. 2144–2151.
  107. Yan H, Gao W, Pan Z, Zhang F, Fan C. The expression of α-SMA in the painful traumatic neuroma: potential role in the pathobiology of neuropathic pain.. J Neurotrauma 2012 Dec 10;29(18):2791-7.
    doi: 10.1089/neu.2012.2502pubmed: 23020218google scholar: lookup
  108. Li J., Wang Y., Wang C., Tai Y., Qian J., Yang J., Wang C., Li J., Huang F.. DSFD: Dual Shot Face Detector. Proceedings of the 2019 IEEE/CVF Conference on Computer Vision and Pattern Recognition (CVPR); Long Beach, CA, USA. 15–20 June 2019; pp. 5055–5064.
  109. Rashid M., Gu X., Lee Y.J.. Interspecies Knowledge Transfer for Facial Keypoint Detection. Proceedings of the 2017 IEEE Conference on Computer Vision and Pattern Recognition (CVPR); Honolulu, HI, USA. 21–26 July 2017; pp. 1600–1609.
  110. Li Z., Broome S., Andersen P.H., Kjellstrom H.. Automated Detection of Equine Facial Action Units.. arXiv 20212102.08983.
  111. Lu Y., Mahmoud M., Robinson P.. Estimating Sheep Pain Level Using Facial Action Unit Detection. Proceedings of the 2017 12th Ieee International Conference on Automatic Face and Gesture Recognition; Washington, DC, USA. 30 May–3 June 2017; pp. 394–399.
    doi: 10.1109/fg.2017.56google scholar: lookup
  112. Hummel H.I., Pessanha F., Salah A.A., van Loon T.J.P.A.M., Veltkamp R.C.. Automatic Pain Detection on Horse and Donkey Faces. Proceedings of the 2020 15th IEEE International Conference on Automatic Face and Gesture Recognition (FG 2020); Buenos Aires, Argentina. 16–20 November 2020; pp. 793–800.
  113. Pessanha F., McLennan K., Mahmoud M.. Towards automatic monitoring of disease progression in sheep: A hierarchical model for sheep facial expressions analysis from video. Proceedings of the 2020 15th IEEE International Conference on Automatic Face and Gesture Recognition (FG 2020); Buenos Aires, Argentina. 16–20 November 2020; pp. 387–393.
  114. Zhao K., Chu W., Zhang H.. Deep Region and Multi-label Learning for Facial Action Unit Detection. Proceedings of the 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR); Las Vegas, NV, USA. 27–30 June 2016; pp. 3391–3399.
  115. Rodriguez P, Cucurull G, Gonzalez J, Gonfaus JM, Nasrollahi K, Moeslund TB, Roca FX. Deep Pain: Exploiting Long Short-Term Memory Networks for Facial Expression Classification.. IEEE Trans Cybern 2022 May;52(5):3314-3324.
    doi: 10.1109/TCYB.2017.2662199pubmed: 28207407google scholar: lookup
  116. Krumhuber E.G., Kappas A., Manstead A.S.R.. Effects of Dynamic Aspects of Facial Expressions: A Review.. Emot. Rev. 2013;5:41–46.
    doi: 10.1177/1754073912451349google scholar: lookup
  117. Broomé S., Gleerup K.B., Haubro Andersen P., Kjellström H.. Dynamics are Important for the Recognition of Equine Pain in Video. Proceedings of the IEEE/CVF Conference on Computer Vision and Pattern Recognition (CVPR); Long Beach, CA, USA. 15–20 June 2019; pp. 12659–12668.
  118. Tuttle AH, Molinaro MJ, Jethwa JF, Sotocinal SG, Prieto JC, Styner MA, Mogil JS, Zylka MJ. A deep neural network to assess spontaneous pain from mouse facial expressions.. Mol Pain 2018 Jan-Dec;14:1744806918763658.
    doi: 10.1177/1744806918763658pmc: PMC5858615pubmed: 29546805google scholar: lookup
  119. Selvaraju R.R., Cogswell M., Das A., Vedantam R., Parikh D., Batra D.. Grad-CAM: Visual Explanations from Deep Networks via Gradient-Based Localization. Proceedings of the 2017 IEEE International Conference on Computer Vision (ICCV); Venice, Italy. 22–29 October 2017; pp. 618–626.
  120. Lloyd A.S., Martin J.E., Bornett-Gauci H.L.I., Wilkinson R.G.. Horse personality: Variation between breeds.. Appl. Anim. Behav. Sci. 2008;112:369–383.
  121. Hausberger M., Fureix C., Lesimple C.. Detecting horses’ sickness: In search of visible signs.. Appl. Anim. Behav. Sci. 2016;175:41–49.
  122. Fureix C, Jego P, Henry S, Lansade L, Hausberger M. Towards an ethological animal model of depression? A study on horses.. PLoS One 2012;7(6):e39280.

Citations

This article has been cited 12 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. Boneh-Shitrit T, Feighelstein M, Bremhorst A, Amir S, Distelfeld T, Dassa Y, Yaroshetsky S, Riemer S, Shimshoni I, Mills DS, Zamansky A. Explainable automated recognition of emotional states from canine facial expressions: the case of positive anticipation and frustration.. Sci Rep 2022 Dec 30;12(1):22611.
    doi: 10.1038/s41598-022-27079-wpubmed: 36585439google scholar: lookup
  3. Gris VN, Broche N Jr, Kaneko A, Okamoto M, Suzuki J, Mills DS, Miyabe-Nishiwaki T. Investigating subtle changes in facial expression to assess acute pain in Japanese macaques.. Sci Rep 2022 Nov 16;12(1):19675.
    doi: 10.1038/s41598-022-23595-xpubmed: 36385151google scholar: lookup
  4. Ren Y, Huang Y, Wang Y, Zhang S, Qu H, Ma J, Wang L, Li L. A High-Performance Day-Age Classification and Detection Model for Chick Based on Attention Encoder and Convolutional Neural Network.. Animals (Basel) 2022 Sep 15;12(18).
    doi: 10.3390/ani12182425pubmed: 36139285google scholar: lookup
  5. Nielsen SS, Alvarez J, Bicout DJ, Calistri P, Canali E, Drewe JA, Garin-Bastuji B, Gonzales Rojas JL, Gortázar Schmidt C, Michel V, Miranda Chueca MÁ, Padalino B, Pasquali P, Roberts HC, Spoolder H, Stahl K, Velarde A, Viltrop A, Winckler C, Earley B, Edwards S, Faucitano L, Marti S, Miranda de La Lama GC, Costa LN, Thomsen PT, Ashe S, Mur L, Van der Stede Y, Herskin M. Welfare of equidae during transport.. EFSA J 2022 Sep;20(9):e07444.
    doi: 10.2903/j.efsa.2022.7444pubmed: 36092762google scholar: lookup
  6. Topczewska J, Bartman J, Kwater T. Assessing the utility value of Hucul horses using classification models, based on artificial neural networks.. PLoS One 2022;17(7):e0271340.
    doi: 10.1371/journal.pone.0271340pubmed: 35881630google scholar: lookup
  7. Feighelstein M, Shimshoni I, Finka LR, Luna SPL, Mills DS, Zamansky A. Automated recognition of pain in cats.. Sci Rep 2022 Jun 10;12(1):9575.
    doi: 10.1038/s41598-022-13348-1pubmed: 35688852google scholar: lookup
  8. Satoła A, Łuszczyński J, Petrych W, Satoła K. Body Weight Prediction from Linear Measurements of Icelandic Foals: A Machine Learning Approach.. Animals (Basel) 2022 May 11;12(10).
    doi: 10.3390/ani12101234pubmed: 35625080google scholar: lookup
  9. Correia-Caeiro C, Burrows A, Wilson DA, Abdelrahman A, Miyabe-Nishiwaki T. CalliFACS: The common marmoset Facial Action Coding System.. PLoS One 2022;17(5):e0266442.
    doi: 10.1371/journal.pone.0266442pubmed: 35580128google scholar: lookup
  10. Broomé S, Ask K, Rashid-Engström M, Haubro Andersen P, Kjellström H. Sharing pain: Using pain domain transfer for video recognition of low grade orthopedic pain in horses.. PLoS One 2022;17(3):e0263854.
    doi: 10.1371/journal.pone.0263854pubmed: 35245288google scholar: lookup
  11. Mota-Rojas D, Marcet-Rius M, Ogi A, Hernández-Ávalos I, Mariti C, Martínez-Burnes J, Mora-Medina P, Casas A, Domínguez A, Reyes B, Gazzano A. Current Advances in Assessment of Dog's Emotions, Facial Expressions, and Their Use for Clinical Recognition of Pain.. Animals (Basel) 2021 Nov 22;11(11).
    doi: 10.3390/ani11113334pubmed: 34828066google scholar: lookup
  12. Lencioni GC, de Sousa RV, de Souza Sardinha EJ, Corrêa RR, Zanella AJ. Pain assessment in horses using automatic facial expression recognition through deep learning-based modeling.. PLoS One 2021;16(10):e0258672.
    doi: 10.1371/journal.pone.0258672pubmed: 34665834google scholar: lookup