Elevated Sensitivity to Tactile Stimuli in Stereotypic Horses.
Abstract: Although stereotypic behaviors are a common problem in captive animals, why certain individuals are more prone to develop them remains elusive. In horses, individuals show considerable differences in how they perceive and react to external events, suggesting that this may partially account for the emergence of stereotypies in this species. In this study, we focused on crib-biting, the most common stereotypy displayed by horses. We compared how established crib-biters ("CB" = 19) and normal controls ("C" = 18) differed in response to a standard "personality" assessment test battery, i.e., reactivity to humans, tactile sensitivity, social reactivity, locomotor activity, and curiosity vs. fearfulness (both in novel and suddenness situations). Our analyses showed that crib-biters only differed from control horses in their tactile sensitivity, suggesting an elevated sensitivity to tactile stimuli. We suggest that this higher tactile sensitivity could be due to altered dopamine or endogenous opioid physiology, resulting from chronic stress exposition. We discuss these findings in relation to the hypothesis that there may be a genetic predisposition for stereotypic behavior in horses, and in relation to current animal husbandry and management practices.
Publication Date: 2019-05-31 PubMed ID: 31275947PubMed Central: PMC6593280DOI: 10.3389/fvets.2019.00162Google 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.
- 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 focuses on crib-biting, a common stereotypy displayed by horses, investigating the potential causes, and identifying that crib-biters were shown to have an elevated tactile sensitivity, possibly due to chronic stress or genetic predisposition.
Methodology
- The researchers conducted a study by comparing how crib-biters and control horses without the stereotypy reacted differently to a standard personality assessment test battery.
- The assessment included measuring the horses’ reactivity to humans, their tactile sensitivity, social reactivity, locomotor activity, and their balance of curiosity vs fearfulness in novel and suddenness situations.
Findings: Increased Tactile Sensitivity
- The results of the study indicated that crib-biters differed from the control horses only in their tactile sensitivity.
- Tactile sensitivity refers to the sensitivity of the horse’s sense of touch and the researchers identified an elevated level of this sensitivity in crib-biting horses.
- This finding implies that an increased sensitivity to touch could be a characteristic of horses that exhibit the crib-biting stereotypy, suggesting this could be contributing to the development of the behavior.
Potential Causes & Implications
- The study proposed that such heightened tactile sensitivity could result from altered dopamine or endogenous opioid physiology. This alteration may be caused due to chronic stress exposition that animals experience in their captive environments.
- The researchers also suggested that the findings may support the hypothesis that there may be a genetic predisposition for stereotypic behavior in horses. This could mean some horses are inherently more likely to develop these behaviors than others.
- The findings underpin the importance of considering the individual sensitivity differences and possible genetic predispositions in horses when developing animal husbandry and management practices, as these could potentially influence the development of stereotypic behaviors such as crib-biting.
Cite This Article
APA
Briefer Freymond S, Bardou D, Beuret S, Bachmann I, Zuberbühler K, Briefer EF.
(2019).
Elevated Sensitivity to Tactile Stimuli in Stereotypic Horses.
Front Vet Sci, 6, 162.
https://doi.org/10.3389/fvets.2019.00162 Publication
Researcher Affiliations
- Agroscope, Swiss National Stud Farm, Avenches, Switzerland.
- Agroscope, Swiss National Stud Farm, Avenches, Switzerland.
- Faculty of Science, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.
- Agroscope, Swiss National Stud Farm, Avenches, Switzerland.
- Faculty of Science, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland.
- School of Psychology and Neuroscience, University of St. Andrews, St. Andrews, Scotland.
- Institute of Agricultural Sciences, ETH Zürich, Zurich, Switzerland.
References
This article includes 103 references
- Mason G, Latham N. Can't stop, won't stop: is stereotypy a reliable animal welfare indicator?. Anim Welf (2004) 13, 57–69.
- McBride SD, Parker MO. The disrupted basal ganglia and behavioural control: an integrative cross-domain perspective of spontaneous stereotypy.. Behav Brain Res 2015 Jan 1;276:45-58.
- Spruijt BM, van den Bos R, Pijlman FT. A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems.. Appl Anim Behav Sci 2001 Apr 26;72(2):145-171.
- Dodman NH, Shuster L, Court MH, Dixon R. Investigation into the use of narcotic antagonists in the treatment of a stereotypic behavior pattern (crib-biting) in the horse.. Am J Vet Res 1987 Feb;48(2):311-9.
- McBride SD, Hemmings A. Altered mesoaccumbens and nigro-striatal dopamine physiology is associated with stereotypy development in a non-rodent species.. Behav Brain Res 2005 Apr 15;159(1):113-8.
- Parker M, McBride SD, Redhead ES, Goodwin D. Differential place and response learning in horses displaying an oral stereotypy.. Behav Brain Res 2009 Jun 8;200(1):100-5.
- Ijichi CL, Collins LM, Elwood RW. Evidence for the role of personality in stereotypy predisposition. Anim Behav (2013) 85:1145–51.
- Bates JE. Concepts and measures of temperament, in Temperament in Childhood. Oxford: John Wiley and Sons; (1989). p. 3–26.
- Goldsmith HH, Buss AH, Plomin R, Rothbart MK, Thomas A, Chess S, Hinde RA, McCall RB. Roundtable: what is temperament? Four approaches.. Child Dev 1987 Apr;58(2):505-29.
- Gosling SD. From mice to men: what can we learn about personality from animal research?. Psychol Bull 2001 Jan;127(1):45-86.
- Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. Integrating animal temperament within ecology and evolution.. Biol Rev Camb Philos Soc 2007 May;82(2):291-318.
- Kilgour R. The open-field test as an assessment of the temperament of dairy cows. Anim Behav (1975) 23:615–24.
- Seaman SC, Davidson HPB, Waran NK. How reliable is temperament assessment in the domestic horse (Equus caballus). Appl Anim Behav Sci (2002) 78:175–91.
- Borstel U. Assessing and influencing personality for improvement of animal welfare: a review of equine studies. CAB Rev (2013) 8:1–27.
- Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R. Animal personality: what are behavioural ecologists measuring?. Biol Rev Camb Philos Soc 2013 May;88(2):465-75.
- Toates F. Cognition, motivation, emotion and action: a dynamic and vulnerable interdependence. Appl Anim Behav Sci (2004) 86:173–204.
- Mason G, Rushen J. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare. 2nd ed. Wallingford: CAB Interantional; (2006).
- Clubb R, Mason G. Animal welfare: captivity effects on wide-ranging carnivores.. Nature 2003 Oct 2;425(6957):473-4.
- McGreevy PD, Cripps PJ, French NP, Green LE, Nicol CJ. Management factors associated with stereotypic and redirected behaviour in the thoroughbred horse.. Equine Vet J 1995 Mar;27(2):86-91.
- Sambraus H. Mouth-based anomalous syndromes. Ethol Farm Anim (1985):391–422.
- Odberg FO. The influence of cage size and environmental enrichment on the development of stereotypies in bank voles (Clethrionomys glareolus).. Behav Processes 1987 Apr;14(2):155-73.
- Gottlieb DH, Capitanio JP, McCowan B. Risk factors for stereotypic behavior and self-biting in rhesus macaques (Macaca mulatta): animal's history, current environment, and personality.. Am J Primatol 2013 Oct;75(10):995-1008.
- Vandeleest JJ, McCowan B, Capitanio JP. Early rearing interacts with temperament and housing to influence the risk for motor stereotypy in rhesus monkeys (Macaca mulatta).. Appl Anim Behav Sci 2011 Jun 1;132(1-2):81-89.
- Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E. Stress revisited: a critical evaluation of the stress concept.. Neurosci Biobehav Rev 2011 Apr;35(5):1291-301.
- Joshi S, Pillay N. Association between personality and stereotypic behaviours in the African striped mouse (Rhabdomys dilectus). Appl Anim Behav Sci (2016) 174:154–61.
- Koolhaas JM, de Boer SF, Coppens CM, Buwalda B. Neuroendocrinology of coping styles: towards understanding the biology of individual variation.. Front Neuroendocrinol 2010 Jul;31(3):307-21.
- Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MA, Blokhuis HJ. Coping styles in animals: current status in behavior and stress-physiology.. Neurosci Biobehav Rev 1999 Nov;23(7):925-35.
- Briefer Freymond S, Bardou D, Briefer EF, Bruckmaier R, Fouché N, Fleury J, Maigrot AL, Ramseyer A, Zuberbühler K, Bachmann I. The physiological consequences of crib-biting in horses in response to an ACTH challenge test.. Physiol Behav 2015 Nov 1;151:121-8.
- Hothersall B, Nicol C. Effects of diet on behavior–normal and abnormal. In: Equine Applied and Clinical Nutrition: Health, Welfare and Performance. Edinburgh: Saunders Elsevier; (2013) 443–44454.
- Williams J, Randle H. Is the expression of stereotypic behavior a performance-limiting factor in animals?. J of Vet Behav (2017) 20:1–10.
- Albright JD, Mohammed HO, Heleski CR, Wickens CL, Houpt KA. Crib-biting in US horses: breed predispositions and owner perceptions of aetiology.. Equine Vet J 2009 May;41(5):455-8.
- Bachmann I, Audigé L, Staᆲher M. Risk factors associated with behavioural disorders of crib-biting, weaving and box-walking in Swiss horses.. Equine Vet J 2003 Mar;35(2):158-63.
- Bachmann I, Staᆲher M. [Housing and use of horses in Switzerland: a representative analysis of the status quo].. Schweiz Arch Tierheilkd 2002 Jul;144(7):331-47.
- Luescher UA, McKeown DB, Dean H. A cross-sectional study on compulsive behaviour (stable vices) in horses.. Equine Vet J Suppl 1998 Nov;(27):14-8.
- McGreevy PD, French NP, Nicol CJ. The prevalence of abnormal behaviours in dressage, eventing and endurance horses in relation to stabling.. Vet Rec 1995 Jul 8;137(2):36-7.
- Mills DS, Alston RD, Rogers V, Longford NT. Factors associated with the prevalence of stereotypic behaviour amongst Thoroughbred horses passing through auctioneer sales. Appl Anim Behav Sci (2002) 78:115–24.
- Waters AJ, Nicol CJ, French NP. Factors influencing the development of stereotypic and redirected behaviours in young horses: findings of a four year prospective epidemiological study.. Equine Vet J 2002 Sep;34(6):572-9.
- Lesimple C, Hausberger M. How accurate are we at assessing others' well-being? The example of welfare assessment in horses.. Front Psychol 2014;5:21.
- Sarrafchi A, Blokhuis HJ. Equine stereotypic behaviors: causation, occurrence, and prevention. J of Vet Behav (2013) 8:386–94.
- Nicol C. Understanding equine stereotypies.. Equine Vet J Suppl 1999 Apr;(28):20-5.
- Roberts K, Hemmings AJ, McBride SD, Parker MO. Causal factors of oral versus locomotor stereotypy in the horse. J of Vet Behav (2017) 20:37–43.
- Bachmann I, Bernasconi P, Herrmann R, Weishaupt MA, Staᆲher M. Behavioural and physiological responses to an acute stressor in crib-biting and control horses. Appl Anim Behav Sci (2003b) 82:297–311.
- Nicol CJ, Badnell-Waters AJ, Bice R, Kelland A, Wilson AD, Harris PA. The effects of diet and weaning method on the behaviour of young horses. Appl Anim Behav Sci (2005) 95:205–21.
- Hemmann K, Raekallio M, Vainio O, Juga J. Crib-biting and its heritability in Finnhorses. Appl Anim Behav Sci (2014) 156:37–43.
- Hosoda T. On the heritability of susceptibility to wind-sucking in horses. Jpn J Zootech Sci (1950) 21:25.
- Mills DS. Repetitive movement problems in the horse. In: Mills DS, Mc, Donnell SM. editors. The Domestic Horse: The Origins, Development and Managment of Ist Behaviour. London: Cambridge Univeristy Press; (2005). p 212–27.
- Vecchiotti GG, Roberto G. Evidence of heredity of cribbing, weawingand stall-walking in thoroughbred horses. Livestock Prod (1986) 14:91–5.
- Momozawa Y. Assessment of equine temperament by a questionnaire survey to caretakers and evaluation of its reliability by simultaneous behavior test. Appl Anim Behav Sci (2003). 84:127–38.
- Munsters CC, Visser EK, van den Broek J, Sloet van Oldruitenborgh-Oosterbaan MM. Physiological and behavioral responses of horses during police training.. Animal 2013 May;7(5):822-7.
- Sian Lloyd A, Elizabeth Martin J, Louise Imogen Bornett-Gauci H, Wilkinson R. Evaluation of a novel method of horse personality assessment: rater-agreement and links to behaviour. Appl Anim Behav Sci 105:205–22 (2007).
- Sian Lloyd A, Elizabeth Martin J, Louise Imogen Bornett-Gauci H, Wilkinson R. Horse personality: variation between breeds. Appl Anim Behav Sci 112:369–83 (2008).
- Søndergaard E, Halekoh U. Young horses' reactions to humans in relation to handling and social environment. Appl Anim Behav Sci (2003) 84:265–80.
- Visser EK, van Reenen CG, van der Werf JT, Schilder MB, Knaap JH, Barneveld A, Blokhuis HJ. Heart rate and heart rate variability during a novel object test and a handling test in young horses.. Physiol Behav 2002 Jun 1;76(2):289-96.
- Wolff A, Hausberger M. Behaviour of foals before weaning may have some genetic basis. Ethology (1994) 96:1–10.
- Wolff A, Hausberger M, Le Scolan N. Experimental tests to assess emotionality in horses.. Behav Processes 1997 Sep;40(3):209-21.
- Nagy K, Bodó G, Bárdos G, Bánszky N, Kabai P. Differences in temperament traits between crib-biting and control horses. Appl Anim Behav Sci (2010) 122:41–7.
- Roberts K, Hemmings AJ, Moore-Colyer M, Parker MO, McBride SD. Neural modulators of temperament: A multivariate approach to personality trait identification in the horse.. Physiol Behav 2016 Dec 1;167:125-131.
- Schork IG, de Azevedo CS, Young RJ. Personality, abnormal behaviour, and health: An evaluation of the welfare of police horses.. PLoS One 2018;13(9):e0202750.
- Lansade L. Le Tempérament du Cheval: étude Théorique: Application à la Sélection des Chevaux Destinés à L'équitation. Tours: University of Tours; (2005).
- Lansade L, Bouissou MF. Reactivity to humans: a temperament trait of horses which is stable across time and situations. Appl Anim Behav Sci (2008) 114:492–508.
- Lansade L, Bouissou MF, Erhard HW. Fearfulness in horses: a temperament trait stable across time and situations. Appl Anim Behav Sci (2008a) 115:182–200.
- Lansade L, Pichard G, Leconte M. Sensory sensitivities: components of a horse's temperament dimension. Appl Anim Behav Sci (2008c) 114:534–53.
- Lansade L, Bouissou MF, Erhard HW. Reactivity to isolation and association with conspecifics: a temperament trait stable across time and situations. Appl Anim Behav Sci (2008b) 109:355–73.
- Finkemeier MA, Langbein J, Puppe B. Personality Research in Mammalian Farm Animals: Concepts, Measures, and Relationship to Welfare.. Front Vet Sci 2018;5:131.
- Górecka-Bruzda A, Jastrzebska E, Sosnowska Z, Jaworski Z, Jezierski T, Chruszczewski MH. Reactivity to humans and fearfulness tests: field validation in polish cold blood horses. Appl Anim Behav Sci (2011) 133:207–15.
- Reimert I, Rodenburg TB, Ursinus WW, Kemp B, Bolhuis JE. Selection based on indirect genetic effects for growth, environmental enrichment and coping style affect the immune status of pigs.. PLoS One 2014;9(9):e108700.
- Huffman JC, Stern TA. Assessment of the Awake but Unresponsive Patient.. Prim Care Companion J Clin Psychiatry 2003 Oct;5(5):227-231.
- 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.
- Lebelt D, Zanella AJ, Unshelm J. Physiological correlates associated with cribbing behaviour in horses: changes in thermal threshold, heart rate, plasma beta-endorphin and serotonin.. Equine Vet J Suppl 1998 Nov;(27):21-7.
- Briefer EF, Maigrot AL, Mandel R, Freymond SB, Bachmann I, Hillmann E. Segregation of information about emotional arousal and valence in horse whinnies.. Sci Rep 2015 Apr 21;4:9989.
- Bove G. Mechanical sensory threshold testing using nylon monofilaments: the pain field's "tin standard".. Pain 2006 Sep;124(1-2):13-7.
- Saslow CA. Understanding the perceptual world of horses. Appl Anim Behav Sci (2002) 78:209–24.
- Briefer EF, Mandel R, Maigrot AL, Briefer Freymond S, Bachmann I, Hillmann E. Perception of emotional valence in horse whinnies.. Front Zool 2017;14:8.
- Landers R. Computing Intraclass Correlations (ICC) as Estimates of Interrater Reliability in SPSS. The Winnower (2015).
- Landers R. Computing (ICC) as intraclass estimates correlations of interrater reliability in SPSS. The Winnower (2015) 2:e14351881744.
- Cicchetti DV. Multiple comparison methods: establishing guidelines for their valid application in neuropsychological research.. J Clin Exp Neuropsychol 1994 Feb;16(1):155-61.
- Pinheiro JC, Bates DM. Mixed-Effects Models in S and S-PLUS. New York, NY: Springer-Verlag; (2000).
- R Development Core Team. R Foundation for Statistical Computing. Vienna (2013).
- Haubo R, Christensen B. A Tutorial on Fitting Cumulative Link Mixed Models With clmm2 from the Ordinal Package. (2019) Available online at: https://cran.r-project.org/web/packages/ordinal/vignettes/clmm2_tutorial.pdf.
- Nagy K, Bodo G, Bardos G, Harnos A, Kabai P. The effect of a feeding stress-test on the behaviour and heart rate variability of control and crib-biting horses (with or without inhibition). Appl Anim Behav Sci (2009) 121:140–7.
- Squibb K, Griffin K, Favier R, Ijichi C. Poker face: discrepancies in behaviour and affective states in horses during stressful handling procedures. Appl Anim Behav Sci (2018) 202:34–8.
- Hausberger M, Müller C. A brief note on some possible factors involved in the reactions of horses to humans. Appl Anim Behav Sci (2002) 76:339–44.
- Blakemore SJ, Tavassoli T, Calò S, Thomas RM, Catmur C, Frith U, Haggard P. Tactile sensitivity in Asperger syndrome.. Brain Cogn 2006 Jun;61(1):5-13.
- Talay-Ongan A, Wood K. Unusual sensory sensitivities in autism: a possible crossroads. Int J Disabil Dev Educ (2000) 47:201–12.
- Frith C. What do imaging studies tell us about the neural basis of autism?. Novartis Found Symp 2003;251:149-66; discussion 166-76, 281-97.
- Plaisted K, O'Riordan M, Baron-Cohen S. Enhanced visual search for a conjunctive target in autism: a research note.. J Child Psychol Psychiatry 1998 Jul;39(5):777-83.
- Harlow HF, Suomi SJ. Induced depression in monkeys.. Behav Biol 1974 Nov;12(3):273-96.
- Dunn W. The sensations of everyday life: empirical, theoretical, and pragmatic considerations.. Am J Occup Ther 2001 Nov-Dec;55(6):608-20.
- Cabib S, Puglisi-Allegra S. The mesoaccumbens dopamine in coping with stress.. Neurosci Biobehav Rev 2012 Jan;36(1):79-89.
- Reinig S, Driever W, Arrenberg AB. The Descending Diencephalic Dopamine System Is Tuned to Sensory Stimuli.. Curr Biol 2017 Feb 6;27(3):318-333.
- McBride S, Hemmings A. A neurologic perspective of equine stereotypy. J Equine Vet Sci (2009) 29:10–6.
- Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw.. J Neurosci Methods 1994 Jul;53(1):55-63.
- Lindegaard C, Vaabengaard D, Christophersen MT, Ekstøm CT, Fjeldborg J. Evaluation of pain and inflammation associated with hot iron branding and microchip transponder injection in horses.. Am J Vet Res 2009 Jul;70(7):840-7.
- Rédua MA, Valadão CA, Duque JC, Balestrero LT. The pre-emptive effect of epidural ketamine on wound sensitivity in horses tested by using von Frey filaments.. Vet Anaesth Analg 2002 Oct;29(4):200-206.
- Kennes D, Odberg FO, Bouquet Y, De Rycke PH. Changes in naloxone and haloperidol effects during the development of captivity-induced jumping stereotypy in bank voles.. Eur J Pharmacol 1988 Aug 9;153(1):19-24.
- Rushen J, De Passillé AM, Schouten W. Stereotypic behavior, endogenous opioids, and postfeeding hypoalgesia in pigs.. Physiol Behav 1990 Jul;48(1):91-6.
- Gillham SB, Dodman NH, Shuster L, Kream R, Rand W. The effect of diet on cribbing behavior and plasma β-endorphin in horses. Appl Anim Behav Sci (1994) 41:147–53.
- Pell SM, McGreevy PD. A study of cortisol and beta-endorphin levels in stereotypic and normal Thoroughbreds. Appl Anim Behav Sci (1999) 64:81–90.
- Hemmings A, Parker MO, Hale C, McBride SD. Causal and functional interpretation of mu- and delta-opioid receptor profiles in mesoaccumbens and nigrostriatal pathways of an oral stereotypy phenotype.. Behav Brain Res 2018 Nov 1;353:108-113.
- Würbel H, Staᆲher M. Standard-haltung für labormäuse–probleme und lösungsansätze. Tierlaboratorium (1994) 17:109–18.
- Minero M, Canali E, Ferrante V, Verga M, Odberg FO. Heart rate and behavioural responses of crib-biting horses to two acute stressors.. Vet Rec 1999 Oct 9;145(15):430-3.
- Ladewig J. Endocrine aspects of stress: evaluation of stress reactions in farm animals. In: Wiepkema PR, Van Adrichem PWM. editors. Biology of Stress in Farm Animals: An Integrative Approach: A Seminar in the CEC Programme of Coordination Research on Animal Welfare, Held on April 17–18:1986, at the Pietersberg Conference Centre, Oosterbeek, The Netherlands. Dordrecht: Springer; (1987). p. 13–25.
- Wathan J, Burrows AM, Waller BM, McComb K. EquiFACS: The Equine Facial Action Coding System.. PLoS One 2015;10(8):e0131738.
Citations
This article has been cited 2 times.- Neethirajan S, Reimert I, Kemp B. Measuring Farm Animal Emotions-Sensor-Based Approaches.. Sensors (Basel) 2021 Jan 14;21(2).
- Rørvang MV, Nielsen BL, McLean AN. Sensory Abilities of Horses and Their Importance for Equitation Science.. Front Vet Sci 2020;7:633.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists