Cited by 112

The DOI matches its Crossref record; 7 of the 7 references it cites were found in a registry or an index.

Facial expression and oxytocin as possible markers of positive emotions in horses

Lansade, Léa, Nowak, Raymond, Lainé, Anne-Lyse, Leterrier, Christine, Bonneau, Coralie, Parias, Céline, Bertin, Aline·2018·Scientific Reports

Abstract

Behavioural and physiological markers of discrete positive emotions remain little investigated in animals. To characterise new markers in horses, we used tactile stimulations to induce emotional situation of contrasting valence. In the Gentle grooming group (G, N = 13) horses were gently groomed during 11 sessions on the body areas they appreciated the most. Horses in the Standard grooming group (S, N = 14) were groomed using a fixed procedure, reported to induce avoidance reactions in some horses. At session 11, G horses expressed significantly more contact-seeking behaviours than S horses, which expressed significantly more avoidance behaviours. This result suggests positive emotions in G horses and negative emotions in S horses. Blood cortisol, oxytocin, heart rate and heart rate variability never differed between before and after the grooming session. However, after the 11 sessions, basal oxytocin levels were lower in the G than in the S group. This difference was unexpected, but supports studies showing that a low level of basal oxytocin could be a marker of better well-being. Analyses of facial expressions during grooming revealed significant differences between groups. These expressions appear to be more sensitive than behavioural indicators because they alone enabled differentiating emotions according to the group when horses were re-exposed to neutral grooming one year after the treatment.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41598-018-32993-z

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • There is evidence indicating that an increase in oxytocin does not necessarily equal good welfare.

    “There is evidence, however, indicating that an increase in oxytocin does not necessarily equal good welfare.”

    From Therapy Dog Welfare Revisited: A Review of the Literature (2021) · cites this paper as [95]

  • In horses, higher basal oxytocin has been observed in individuals that displayed mimic muscle activity associated with discomfort.

    “In horses, higher basal oxytocin has been observed in individuals that displayed mimic muscle activity associated with discomfort [95].”

    From Therapy Dog Welfare Revisited: A Review of the Literature (2021) · cites this paper as [95]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 61

  1. Russell, J. A circumplex model of affect. J. Pers. Soc. Psychol. 39, 1161–1178 (1980). · DOI · Paper page
  2. Reefmann, N., Wechsler, B. & Gygax, L. Behavioural and physiological assessment of positive and negative emotion in sheep. Anim. Behav. 78, 651–659 (2009). · DOI
  3. Mendl, M., Burman, O. H. P. & Paul, E. S. An integrative and functional framework for the study of animal emotion and mood. Proc. R. Soc. B 277, 2895–2904 (2010). · DOI · Paper page
  4. Fridlund, A. J. Evolution and facial action in reflex, social motive, and paralanguage. Biol. Psychol. 32, 3–100 (1991). · DOI
  5. Waller, B. M. & Micheletta, J. Facial Expression in Nonhuman Animals. Emot. Rev. 5, 54–59 (2013). · DOI
  6. Miller, A. L., Kitson, G. L., Skalkoyannis, B., Flecknell, P. A. & Leach, M. C. Using the mouse grimace scale and behaviour to assess pain in CBA mice following vasectomy. Appl. Anim. Behav. Sci. 181, 160–165 (2016). · DOI
  7. McLennan, K. M. et al. Development of a facial expression scale using footrot and mastitis as models of pain in sheep. Appl. Anim. Behav. Sci. 176, 19–26 (2016). · DOI
  8. Hageri, C. et al. The Sheep Grimace Scale as an indicator of post-operative distress and pain in laboratory sheep. PLoS ONE 12 (2017). · DOI
  9. Guesgen, M. J. et al. Coding and quantification of a facial expression for pain in lambs. Behav. Processes 132, 49–56 (2016). · DOI
  10. Dalla Costa, E. et al. Development of the Horse Grimace Scale (HGS) as a Pain Assessment Tool in Horses Undergoing Routine Castration. PLoS ONE 9 (2014). · DOI
  11. Gleerup, K. B., Forkman, B., Lindegaard, C. & Andersen, P. H. An equine pain face. Vet Anaesth Analg 42, 103–114 (2015). · DOI
  12. Dalla Costa, E., Bracci, D., Dai, F., Lebelt, D. & Minero, M. Do Different Emotional States Affect the Horse Grimace Scale Score? A Pilot Study. J Equine Vet Sci 54, 114–117 (2017). · DOI
  13. Mullard, J., Berger, J. M., Ellis, A. D. & Dyson, S. Development of an ethogram to describe facial expressions in ridden horses (FEReq). J Vet Behav 18, 7–12 (2017). · DOI
  14. Finlayson, K., Lampe, J. F., Hintze, S., Wurbel, H. & Melotti, L. Facial Indicators of Positive Emotions in Rats. PLoS ONE 11 (2016). · DOI
  15. Proctor, H. S. & Carder, G. Measuring positive emotions in cows: Do visible eye whites tell us anything? Physiol. Behav. 147, 1–6 (2015). · DOI
  16. Lambert, H. S. & Carder, G. Looking into the eyes of a cow: Can eye whites be used as a measure of emotional state? Appl. Anim. Behav. Sci. 186, 1–6 (2017). · DOI
  17. Hintze, S., Smith, S., Patt, A., Bachmann, I. & Wurbel, H. Are Eyes a Mirror of the Soul? What Eye Wrinkles Reveal about a Horse’s Emotional State. PLoS ONE 11 (2016). · DOI
  18. Reefmann, N., Kaszas, F. B., Wechsler, B. & Gygax, L. Ear and tail postures as indicators of emotional valence in sheep. Appl. Anim. Behav. Sci. 118, 199–207 (2009). · DOI
  19. Guesgen, M. J. et al. Lambs show changes in ear posture when experiencing pain. Anim. Welfare 25, 171–177 (2016). · DOI
  20. Proctor, H. S. & Carder, G. Can ear postures reliably measure the positive emotional state of cows? Appl. Anim. Behav. Sci. 161, 20–27 (2014). · DOI
  21. Briefer Freymond, S. et al. Behaviour of horses in a judgment bias test associated with positive or negative reinforcement. Appl. Anim. Behav. Sci. 158, 34–45 (2014). · DOI
  22. Wathan, J., Burrows, A. M., Waller, B. M. & McComb, K. EquiFACS: The Equine Facial Action Coding System. PLoS ONE 10 (2015). · DOI
  23. McDonnell, S. M. & Poulin, A. Equid play ethogram. Appl. Anim. Behav. Sci. 78, 263–290 (2002). · DOI
  24. Minton, J. E. Function of the HPA axis and Sympathetic nervous system in models of acute stress in domestic farm animals. J. Anim. Sci. 72, 1891–1898 (1994). · DOI
  25. Peeters, M., Sulon, J., Serteyn, D. & Vandenheede, M. Assessment of stress level in horses during competition using salivary cortisol: preliminary studies. J Vet Beh 5, 216 (2009). · DOI
  26. Valenchon, M., Lévy, F., Moussu, C. & Lansade, L. Stress affects instrumental learning based on positive or negative reinforcement in interaction with personality in domestic horses. PLoS ONE 12 (2017). · DOI
  27. Steptoe, A., Wardle, J. & Marmot, M. Positive affect and health-related neuroendocrine, cardiovascular, and inflammatory processes. Proc Natl Acad Sci USA 102, 6508–6512 (2005). · DOI · Paper page
  28. Feh, C. & De Mazières, J. Grooming at a preferred site reduces heart rate in horses. Anim. Behav. 46, 1191–1194 (1993). · DOI
  29. Zebunke, M., Langbein, J., Manteuffel, G. & Puppe, B. Autonomic reactions indicating positive affect during acoustic reward learning in domestic pigs. Anim. Behav. 81, 481–489 (2011). · DOI
  30. Briefer, E. F., Tettamanti, F. & McElligott, A. G. Emotions in goats: mapping physiological, behavioural and vocal profiles. Anim. Behav. 99, 131–143 (2015). · DOI
  31. Odendaal, J. S. J. & Meintjes, R. A. Neurophysiological correlates of affiliative behaviour between humans and dogs. Vet. J. 165, 296–301 (2003). · DOI · Paper page
  32. Fortin, M. et al. Emotional state and personality influence cognitive flexibility in horses. J. Comp. Psychol (2018). · DOI
  33. Uvnas-Moberg, K., Arn, I. & Magnusson, D. The psychobiology of emotion: The role of the oxytocinergic system. Int J Behav Med 12, 59–65 (2005). · DOI · Paper page
  34. Coulon, M. et al. Human-lamb bonding: Oxytocin, cortisol and behavioural responses of lambs to human contacts and social separation. Psychoneuroendocrinology 38, 499–508 (2013). · DOI
  35. Pajor, E. A., Rushen, J. & de Passillé, A. M. B. Dairy cattle’s choice of handling treatments in a Y-maze. Appl. Anim. Behav. Sci. 80, 93–107 (2003). · DOI
  36. Westerath, H. S., Gygax, L. & Hillmann, E. Are special feed and being brushed judged as positive by calves? Appl. Anim. Behav. Sci. 156, 12–21 (2014). · DOI
  37. Tamioso, P. R., Rucinque, D. S., Taconeli, C. A., da Silva, G. P. & Molento, C. F. M. Behavior and body surface temperature as welfare indicators in selected sheep regularly brushed by a familiar observer. J Vet Beh 19, 27–34 (2017). · DOI
  38. Schmied, C., Waiblinger, S., Scharl, T., Leisch, F. & Boivin, X. Stroking of different body regions by a human: Effects on behaviour and heart rate of dairy cows. Appl. Anim. Behav. Sci. 109, 25–38 (2008). · DOI · Paper page
  39. Bertenshaw, C. E. & Rowlinson, P. Exploring heifers’ perception of ‘positive’ treatment through their motivation to pursue a retreated human. Anim. Welfare 17, 313–319 (2008). · DOI
  40. Rehn, T., Handlin, L., Uvnas-Moberg, K. & Keeling, L. J. Dogs’ endocrine and behavioural responses at reunion are affected by how the human initiates contact. Physiol. Behav. 124, 45–53 (2014). · DOI
  41. McBride, S. D., Hemmings, A. & Robinson, K. A preliminary study on the effect of massage to reduce stress in the horse. J Equine Vet Sci 24, 76–81 (2004). · DOI
  42. Parr, L. A., Waller, B. M., Burrows, A. M., Gothard, K. M. & Vick, S. J. Brief Communication: MaqFACS: A Muscle-Based Facial Movement Coding System for the Rhesus Macaque. Am. J. Phys. Anthropol. 143, 625–630 (2010). · DOI
  43. Sankey, C., Richard-Yris, M.-A., Leroy, H., Henry, S. & Hausberger, M. Positive interactions lead to lasting positive memories in horses, Equus caballus. Anim. Behav. 79, 869–875 (2010). · DOI
  44. Fedurek, P., Slocombe, K. E., Hartel, J. A. & Zuberbuhler, K. Chimpanzee lip-smacking facilitates cooperative behaviour. Sci Rep 5 (2015). · DOI
  45. Valenchon, M. et al. Stress Modulates Instrumental Learning Performances in Horses (Equus caballus) in Interaction with Temperament. PLoS ONE 8, e62324 (2013). · DOI
  46. Young, T., Creighton, E., Smith, T. & Hosie, C. A novel scale of behavioural indicators of stress for use with domestic horses. Appl. Anim. Behav. Sci. 140, 33–43 (2012). · DOI
  47. Stock, S. & Uvnasmoberg, K. Increased plasma levels of oxytocin in response to afferent electrical stimulation of the sciatic and vagal nerves and in response to touch and pinch in anaesthetized rats. Acta Physiol. Scand. 132, 29–34 (1988). · DOI · Paper page
  48. Handlin, L. et al. Short-Term Interaction between Dogs and Their Owners: Effects on Oxytocin, Cortisol, Insulin and Heart Rate-An Exploratory Study. Anthrozoos 24, 301–315 (2011). · DOI · Paper page
  49. Feldman, R., Gordon, I., Schneiderman, I., Weisman, O. & Zagoory-Sharon, O. Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35, 1133–1141 (2010). · DOI · Paper page
  50. Guesdon, V. et al. Behavioral and endocrine evaluation of the stressfulness of single-pen housing compared to group-housing and social isolation conditions. Physiol. Behav. 147, 63–70 (2015). · DOI
  51. Rault, J. L., van den Munkhof, M. & Buisman-Pijlman, F. T. A. Oxytocin as an Indicator of Psychological and Social Well-Being in Domesticated Animals: A Critical Review. Front Psychol 8 (2017). · DOI
  52. Grippo, A. J. et al. Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinology 32, 966–980 (2007). · DOI · Paper page
  53. Gaudin, S. et al. All bonds are not alike: A psychoendocrine evaluation of infant attachment. Dev. Psychobiol. 60, 90–103 (2018). · DOI
  54. Taylor, S. E. et al. Relation of oxytocin to psychological stress responses and hypothalamic-pituitary-adrenocorticaI axis activity in older women. Psychosom. Med. 68, 238–245 (2006). · DOI · Paper page
  55. Briefer, E. F. et al. Segregation of information about emotional arousal and valence in horse whinnies. Sci Rep 5 (2015). · DOI
  56. Forkman, B., Boissy, A., Meunier-Salauen, M. C., Canali, E. & Jones, R. B. A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiol. Behav. 92, 340–374 (2007). · DOI
  57. Russell, J. A. & Barrett, L. F. Core affect, prototypical emotional episodes, and other things called Emotion: Dissecting the elephant. J. Pers. Soc. Psychol. 76, 805–819 (1999). · DOI
  58. Burgdorf, J. & Panksepp, J. The neurobiology of positive emotions. Neurosci. Biobehav. Rev. 30, 173–187 (2006). · DOI · Paper page
  59. Garamszegi, L. Z. Comparing effect sizes across variables: generalization without the need for Bonferroni correction. Behav. Ecol. 17, 682–687 (2006). · DOI
  60. Garcia, L. V. Escaping the Bonferroni iron claw in ecological studies. Oikos 105, 657–663 (2004). · DOI
  61. Nakagawa, S. A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav. Ecol. 15, 1044–1045 (2004). · DOI

Cited by

Sorted by citations

Metadata

Authors
Lansade, L., Nowak, R., Lainé, A.-L., Leterrier, C., Bonneau, C., Parias, C., & Bertin, A.
Venue
Scientific Reports
Published
2018-10-02
Volume
8
Issue
1
ISSN
2045-2322
Cited by
112
References
7
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review