FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Animals : an open access journal from MDPI2022; 12(20); doi: 10.3390/ani12202818

Habit Formation and the Effect of Repeated Stress Exposures on Cognitive Flexibility Learning in Horses.

Abstract: Horse training exposes horses to an array of cognitive and ethological challenges. Horses are routinely required to perform behaviours that are not aligned to aspects of their ethology, which may delay learning. While horses readily form habits during training, not all of these responses are considered desirable, resulting in the horse being subject to retraining. This is a form of cognitive flexibility and is critical to the extinction of habits and the learning of new responses. It is underpinned by complex neural processes which can be impaired by chronic or repeated stress. Domestic horses may be repeatedly exposed to multiples stressors. The potential contribution of stress impairments of cognitive flexibility to apparent training failures is not well understood, however research from neuroscience can be used to understand horses' responses to training. We trained horses to acquire habit-like responses in one of two industry-style aversive instrumental learning scenarios (moving away from the stimulus-instinctual or moving towards the stimulus-non-instinctual) and evaluated the effect of repeated stress exposures on their cognitive flexibility in a reversal task. We measured heart rate as a proxy for noradrenaline release, salivary cortisol and serum Brain Derived Neurotrophic Factor (BDNF) to infer possible neural correlates of the learning outcomes. The instinctual task which aligned with innate equine escape responses to aversive stimuli was acquired significantly faster than the non-instinctual task during both learning phases, however contrary to expectations, the repeated stress exposure did not impair the reversal learning. We report a preliminary finding that serum BDNF and salivary cortisol concentrations in horses are positively correlated. The ethological salience of training tasks and cognitive flexibility learning can significantly affect learning in horses and trainers should adapt their practices where such tasks challenge innate equine behaviour.
Get Full Text
Publication Date: 2022-10-18 PubMed ID: 36290204PubMed Central: PMC9597801DOI: 10.3390/ani12202818Google 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 paper investigates the concept of habit formation in horses and how continuous exposure to stress can affect the horse’s ability to learn new behaviors and unlearn undesirable ones, a process known as cognitive flexibility. The researchers compared two types of training tasks—instinctual (moving away from stimulus) and non-instinctual (moving towards stimulus), monitoring physiological responses such as heart rate, salivary cortisol, and serum Brain-Derived Neurotrophic Factor (BDNF) levels. Contrary to expectations, repeated stress exposure did not hamper the learning process.

Understanding Cognitive Flexibility in Horses

  • The researchers tried to understand how horses adapt to training tasks that are atypical of their instinctual behavior. Notably, horses are subjected to tasks that often conflict with their inherent ethology, which may impact their learning process.
  • Repetitive training leads to habit formation in horses, but not all habits formed are desirable. Training might need to be undone and relearned, demonstrating cognitive flexibility—an attribute that depends on complex neural processes.
  • However, this cognitive flexibility could be affected by chronic or repeated exposure to stress. Given that domestic horses are often exposed to multiple stressors, comprehending the impact of stress on their cognitive flexibility becomes pivotal.

Research Methodology

  • The researchers trained horses to form habit-like responses using two different industry-related learning scenarios. The instinctual task urged the horse to move away from the stimulus, while the non-instinctual task prompted them towards the stimulus.
  • They evaluated the impact of repeated stress exposures on cognitive flexibility, introducing a role-reversal task. They utilized heart rate as a measure of noradrenaline release, and they analyzed salivary cortisol and serum BDNF to understand potential neural correlates of the resultant learning outcomes.

Key Findings

  • Instinctual tasks, closely aligned with horses’ response mechanisms, were picked up faster than non-instinctual tasks during both learning phases. Interestingly, the recurrence of stress did not negatively influence the secondary learning (reversal learning).
  • Initial findings also indicated a positive correlation between the concentrations of serum BDNF and salivary cortisol in horses, suggesting a potential relationship between these factors and their learning patterns.

Implications and Recommendations

  • The results provide valuable insights into equine learning processes, with a specific focus on habit formation and cognitive flexibility, painting a clearer picture about horses’ responses to repeated stress exposures.
  • The study bolsters the influence of ethological relevance of training tasks on horses’ learning, suggesting that trainers should alter their approaches when tasks go against innate equine behaviour.

Cite This Article

APA
Henshall C, Randle H, Francis N, Freire R. (2022). Habit Formation and the Effect of Repeated Stress Exposures on Cognitive Flexibility Learning in Horses. Animals (Basel), 12(20). https://doi.org/10.3390/ani12202818

Publication

Animals : an open access journal from MDPI
ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 12
Issue: 20

Researcher Affiliations

Henshall, Cathrynne
  • School of Environmental, Agricultural and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2650, Australia.
Randle, Hayley
  • School of Environmental, Agricultural and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2650, Australia.
Francis, Nidhish
  • School of Environmental, Agricultural and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2650, Australia.
Freire, Rafael
  • School of Environmental, Agricultural and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2650, Australia.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 125 references
  1. McGreevy P.D., McLean A.N.. Roles of learning theory and ethology in equitation. J. Vet. Behav. Clin. Appl. Res. 2007;2:108–118.
    doi: 10.1016/j.jveb.2007.05.003google scholar: lookup
  2. McLean A.N., McGreevy P.D.. Horse-training techniques that may defy the principles of learning theory and compromise welfare. J. Vet. Behav. Clin. Appl. Res. 2010;5:187–195.
    doi: 10.1016/j.jveb.2010.04.002google scholar: lookup
  3. Hurtubise J.L., Howland J.G.. Effects of stress on behavioral flexibility in rodents. Neuroscience 2017;345:176–192.
    doi: 10.1016/j.neuroscience.2016.04.007pubmed: 27066767google scholar: lookup
  4. Waring G.H.. Horse Behavior. 2nd ed. Noyes Publications; Norwich, NY, USA: 2003.
  5. McGreevy P., Hahn C.N., McLean A.N.. Equine Behavior: A Guide for Veterinarians and Equine Scientists. Saunders; London, UK: 2004. Equine behavior: A guide for veterinarians and equine scientists; p. xiv + 369.
  6. Campese V.D., Sears R.M., Moscarello J.M., Diaz-Mataix L., Cain C.K., LeDoux J.E.. The Neural Foundations of Reaction and Action in Aversive Motivation. In: Eleanor H., Simpson P., Balsam D., editors. Behavioral Neuroscience of Motivation. Springer International Publishing; Cham, Swizterland: 2016. pp. 171–195.
    pubmed: 26643998
  7. Bolles R.C.. Species-specific defense reactions and avoidance learning. Psychol. Rev. 1970;77:32–48.
    doi: 10.1037/h0028589google scholar: lookup
  8. Panksepp J., Fuchs T., Iacobucci P.. The basic neuroscience of emotional experiences in mammals: The case of subcortical FEAR circuitry and implications for clinical anxiety. Appl. Anim. Behav. Sci. 2011;129:1–17.
    doi: 10.1016/j.applanim.2010.09.014google scholar: lookup
  9. McLean A.N., Christensen J.W.. The application of learning theory in horse training. Appl. Anim. Behav. Sci. 2017;190:18–27.
    doi: 10.1016/j.applanim.2017.02.020google scholar: lookup
  10. Padalino B.. Effects of the different transport phases on equine health status, behavior, and welfare: A review. J. Vet. Behav. Clin. Appl. Res. 2015;10:272–282.
    doi: 10.1016/j.jveb.2015.02.002google scholar: lookup
  11. Munsters C.C.B.M., Visser E.K., Broek J.V.D., van Oldruitenborgh-Oosterbaan M.M.S.. Physiological and behavioral responses of horses during police training. Animal 2013;7:822–827.
    doi: 10.1017/S1751731112002327pubmed: 23244508google scholar: lookup
  12. Padalino B., Henshall C., Raidal S.L., Knight P., Celi P., Jeffcott L., Muscatello G.. Investigations Into Equine Transport-Related Problem Behaviors: Survey Results. J. Equine Vet. Sci. 2016;48:166–173.e162.
    doi: 10.1016/j.jevs.2016.07.001google scholar: lookup
  13. McLean A.. The Truth about Horses. Quarto Publishing; London, UK: 2003.
  14. LeDoux J., Daw N.D.. Surviving threats: Neural circuit and computational implications of a new taxonomy of defensive behaviour. Nat. Rev. Neurosci. 2018;19:269–282.
    doi: 10.1038/nrn.2018.22pubmed: 29593300google scholar: lookup
  15. Maren S.. Seeking a Spotless Mind: Extinction, Deconsolidation, and Erasure of Fear Memory. Neuron 2011;70:830–845.
    doi: 10.1016/j.neuron.2011.04.023pmc: PMC3112357pubmed: 21658578google scholar: lookup
  16. Ressler R.L., Maren S.. Synaptic encoding of fear memories in the amygdala. Curr. Opin. Neurobiol. 2019;54:54–59.
    doi: 10.1016/j.conb.2018.08.012pmc: PMC6361699pubmed: 30216780google scholar: lookup
  17. . Principles of Learning Theory in Equitation. 2018.
  18. McGreevy P., McLean A.. In: Domestic Horse: The Origins, Development and Management of Its Behaviour. Mills D.S., McDonnell S., editors. Cambridge University Press; Cambridge, UK: 2005. pp. 196–211.
  19. Audet J.-N., Lefebvre L.. What’s flexible in behavioral flexibility?. Behav. Ecol. 2017;28:943–947.
    doi: 10.1093/beheco/arx007google scholar: lookup
  20. McBride S.D., Parker M.O., Roberts K., Hemmings A.. Applied neurophysiology of the horse; implications for training, husbandry and welfare. Appl. Anim. Behav. Sci. 2017;190:90–101.
    doi: 10.1016/j.applanim.2017.02.014google scholar: lookup
  21. Yin H.H., Ostlund S.B., Knowlton B.J., Balleine B.W.. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci. 2005;22:513–523.
    doi: 10.1111/j.1460-9568.2005.04218.xpubmed: 16045504google scholar: lookup
  22. Balleine B.W., Liljeholm M., Ostlund S.B.. The integrative function of the basal ganglia in instrumental conditioning. Behav. Brain Res. 2009;199:43–52.
    doi: 10.1016/j.bbr.2008.10.034pubmed: 19027797google scholar: lookup
  23. Corbit L.H., Leung B., Balleine B.. The Role of the Amygdala-Striatal Pathway in the Acquisition and Performance of Goal-Directed Instrumental Actions. J. Neurosci. 2013;33:17682–17690.
    doi: 10.1523/JNEUROSCI.3271-13.2013pmc: PMC6618427pubmed: 24198361google scholar: lookup
  24. Izquierdo A., Brigman J., Radke A., Rí¾ck P., Holmes A.. The neural basis of reversal learning: An updated perspective. Neuroscience 2017;345:12–26.
    doi: 10.1016/j.neuroscience.2016.03.021pmc: PMC5018909pubmed: 26979052google scholar: lookup
  25. Yaple Z.A., Yu R.. Fractionating adaptive learning: A meta-analysis of the reversal learning paradigm. Neurosci. Biobehav. Rev. 2019;102:85–94.
    doi: 10.1016/j.neubiorev.2019.04.006pubmed: 31004627google scholar: lookup
  26. Castro-Alamancos M.A.. Absence of Rapid Sensory Adaptation in Neocortex during Information Processing States. Neuron 2004;41:455–464.
    doi: 10.1016/S0896-6273(03)00853-5pubmed: 14766183google scholar: lookup
  27. Poremba A., Gabriel M.. Amygdala Neurons Mediate Acquisition But Not Maintenance of Instrumental Avoidance Behavior in Rabbits. J. Neurosci. 1999;19:9635–9641.
    doi: 10.1523/JNEUROSCI.19-21-09635.1999pmc: PMC6782919pubmed: 10531465google scholar: lookup
  28. Killcross S.. Coordination of Actions and Habits in the Medial Prefrontal Cortex of Rats. Cereb. Cortex 2003;13:400–408.
    doi: 10.1093/cercor/13.4.400pubmed: 12631569google scholar: lookup
  29. Goldfarb E.V., Phelps E.A.. Stress and the trade-off between hippocampal and striatal memory. Curr. Opin. Behav. Sci. 2017;14:47–53.
    doi: 10.1016/j.cobeha.2016.11.017google scholar: lookup
  30. Quinn J.J., Pittenger C., Lee A.S., Pierson J.L., Taylor J.R.. Striatum-dependent habits are insensitive to both increases and decreases in reinforcer value in mice. Eur. J. Neurosci. 2013;37:1012–1021.
    doi: 10.1111/ejn.12106pmc: PMC3604187pubmed: 23298231google scholar: lookup
  31. Solomon R.L., Kamin L.J., Wynne L.C.. Traumatic avoidance learning: The outcomes of several extinction procedures with dogs. J. Abnorm. Soc. Psychol. 1953;48:291–302.
    doi: 10.1037/h0058943pubmed: 13052353google scholar: lookup
  32. Manning E.E., Bradfield L.A., Iordanova M.D.. Adaptive behaviour under conflict: Deconstructing extinction, reversal, and active avoidance learning. Neurosci. Biobehav. Rev. 2020;120:526–536.
    doi: 10.1016/j.neubiorev.2020.09.030pubmed: 33035525google scholar: lookup
  33. Cain C.K.. Avoidance problems reconsidered. Curr. Opin. Behav. Sci. 2019;26:9–17.
    doi: 10.1016/j.cobeha.2018.09.002pmc: PMC6456067pubmed: 30984805google scholar: lookup
  34. LeDoux J.E., Moscarello J., Sears R., Campese V.. The birth, death and resurrection of avoidance: A reconceptualization of a troubled paradigm. Mol. Psychiatry 2016;22:24–36.
    doi: 10.1038/mp.2016.166pmc: PMC5173426pubmed: 27752080google scholar: lookup
  35. O’Malley J.J., Bruning J.L.. Aversive stimulation and reversal learning. Psychon. Sci. 1969;15:40.
    doi: 10.3758/BF03336187google scholar: lookup
  36. Quirk G.J., Mueller D.. Neural Mechanisms of Extinction Learning and Retrieval. Neuropsychopharmacology 2008;33:56–72.
    doi: 10.1038/sj.npp.1301555pmc: PMC2668714pubmed: 17882236google scholar: lookup
  37. Trapp S., O’Doherty J.P., Schwabe L.. Stressful Events as Teaching Signals for the Brain. Trends Cogn. Sci. 2018;22:475–478.
    doi: 10.1016/j.tics.2018.03.007pubmed: 29655607google scholar: lookup
  38. Iordanova M.D., Yau J.O.-Y., McDannald M.A., Corbit L.H.. Neural substrates of appetitive and aversive prediction error. Neurosci. Biobehav. Rev. 2021;123:337–351.
    doi: 10.1016/j.neubiorev.2020.10.029pmc: PMC7933120pubmed: 33453307google scholar: lookup
  39. Lammel S., Lim B.K., Malenka R.C.. Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology 2014;76:351–359.
    doi: 10.1016/j.neuropharm.2013.03.019pmc: PMC3778102pubmed: 23578393google scholar: lookup
  40. Schultz W.. Dopamine reward prediction error coding. Dialog-Clin. Neurosci. 2016;18:23–32.
    doi: 10.31887/DCNS.2016.18.1/wschultzpmc: PMC4826767pubmed: 27069377google scholar: lookup
  41. Peters A., McEwen B.S., Friston K.. Uncertainty and stress: Why it causes diseases and how it is mastered by the brain. Prog. Neurobiol. 2017;156:164–188.
    doi: 10.1016/j.pneurobio.2017.05.004pubmed: 28576664google scholar: lookup
  42. Wenzel J.M., Rauscher N.A., Cheer J.F., Oleson E.B.. A Role for Phasic Dopamine Release within the Nucleus Accumbens in Encoding Aversion: A Review of the Neurochemical Literature. ACS Chem. Neurosci. 2015;6:16–26.
    doi: 10.1021/cn500255ppmc: PMC5820768pubmed: 25491156google scholar: lookup
  43. Hemmings A., McBride S., Hale C.. Perseverative responding and the aetiology of equine oral stereotypy. Appl. Anim. Behav. Sci. 2007;104:143–150.
    doi: 10.1016/j.applanim.2006.04.031google scholar: lookup
  44. Kirsty R., Andrew H., Meriel M.-C., Catherine H.. Cognitive differences in horses performing locomotor versus oral stereotypic behaviour. Appl. Anim. Behav. Sci. 2015;168:37–44.
    doi: 10.1016/j.applanim.2015.04.015google scholar: lookup
  45. Freymond S.B., Ruet A., Grivaz M., Fuentes C., Zuberbühler K., Bachmann I., Briefer E.F.. Stereotypic horses (Equus caballus) are not cognitively impaired. Anim. Cogn. 2019;22:17–33.
    doi: 10.1007/s10071-018-1217-8pubmed: 30328528google scholar: lookup
  46. Fortin M., Valenchon M., Lévy F., Calandreau L., Arnould C., Lansade L.. Emotional state and personality influence cognitive flexibility in horses (Equus caballus). J. Comp. Psychol. 2018;132:130–140.
    doi: 10.1037/com0000091pubmed: 29517248google scholar: lookup
  47. Lansade L., Marchand A.R., Coutureau E., Ballé C., Polli F., Calandreau L.. Personality and predisposition to form habit behaviours during instrumental conditioning in horses (Equus caballus). PLoS ONE 2017;12:e0171010.
    doi: 10.1371/journal.pone.0171010pmc: PMC5291538pubmed: 28158199google scholar: lookup
  48. McGreevy P., McLean A.. Equitation Science. Wiley Blackwell; London, UK: 2010.
  49. Zhang Y., Shao F., Wang Q., Xie X., Wang W.. Neuroplastic Correlates in the mPFC Underlying the Impairment of Stress-Coping Ability and Cognitive Flexibility in Adult Rats Exposed to Chronic Mild Stress during Adolescence. Neural Plast. 2017;2017:1–10.
    doi: 10.1155/2017/9382797pmc: PMC5274659pubmed: 28182105google scholar: lookup
  50. Jett J.D., Bulin S.E., Hatherall L.C., McCartney C.M., Morilak D.A.. Deficits in cognitive flexibility induced by chronic unpredictable stress are associated with impaired glutamate neurotransmission in the rat medial prefrontal cortex. Neuroscience 2017;346:284–297.
    doi: 10.1016/j.neuroscience.2017.01.017pmc: PMC5344040pubmed: 28131625google scholar: lookup
  51. Hermans E.J., Henckens M.J., Joels M., Fernández G.. Dynamic adaptation of large-scale brain networks in response to acute stressors. Trends Neurosci. 2014;37:304–314.
    doi: 10.1016/j.tins.2014.03.006pubmed: 24766931google scholar: lookup
  52. Shields G.S., Bonner J.C., Moons W.G.. Does cortisol influence core executive functions? A meta-analysis of acute cortisol administration effects on working memory, inhibition, and set-shifting. Psychoneuroendocrinology 2015;58:91–103.
    doi: 10.1016/j.psyneuen.2015.04.017pubmed: 25973565google scholar: lookup
  53. Bondi C., Rodriguez G., Gould G., Frazer A., Morilak D.A.. Chronic Unpredictable Stress Induces a Cognitive Deficit and Anxiety-Like Behavior in Rats that is Prevented by Chronic Antidepressant Drug Treatment. Neuropsychopharmacology 2008;33:320–331.
    doi: 10.1038/sj.npp.1301410pubmed: 17406647google scholar: lookup
  54. Douma E.H., de Kloet E.R.. Stress-induced plasticity and functioning of ventral tegmental dopamine neurons. Neurosci. Biobehav. Rev. 2020;108:48–77.
    doi: 10.1016/j.neubiorev.2019.10.015pubmed: 31666179google scholar: lookup
  55. Padalino B., Raidal S.L., Carter N., Celi P., Muscatello G., Jeffcott L., de Silva K.. Immunological, clinical, haematological and oxidative responses to long distance transportation in horses. Res. Vet. Sci. 2017;115:78–87.
    doi: 10.1016/j.rvsc.2017.01.024pubmed: 28160731google scholar: lookup
  56. Lesimple C.. Indicators of Horse Welfare: State-of-the-Art. Animals 2020;10:294.
    doi: 10.3390/ani10020294pmc: PMC7070675pubmed: 32069888google scholar: lookup
  57. Nogueira G.P., Barnabe R.C.. Is the Thoroughbred race-horse under chronic stress?. Braz. J. Med. Biol. Res. 1997;30:1237–1239.
    doi: 10.1590/S0100-879X1997001000016pubmed: 9496444google scholar: lookup
  58. Alexander S.L., Irvine C.H.G.. The effect of social stress on adrenal axis activity in horses: The importance of monitoring corticosteroid-binding globulin capacity. J. Endocrinol. 1998;157:425–432.
    doi: 10.1677/joe.0.1570425pubmed: 9691975google scholar: lookup
  59. Cousillas H., Oger M., Rochais C., Pettoello C., Ménoret M., Henry S., Hausberger M.. An Ambulatory Electroencephalography System for Freely Moving Horses: An Innovating Approach. Front. Veter-Sci. 2017;4:57.
    doi: 10.3389/fvets.2017.00057pmc: PMC5411420pubmed: 28512633google scholar: lookup
  60. Mott R.O., Hawthorne S.J., McBride S.D.. Blink rate as a measure of stress and attention in the domestic horse (Equus caballus). Sci. Rep. 2020;10:21409.
    doi: 10.1038/s41598-020-78386-zpmc: PMC7722727pubmed: 33293559google scholar: lookup
  61. Schwabe L., Wolf O.T.. Learning under stress impairs memory formation. Neurobiol. Learn. Mem. 2010;93:183–188.
    doi: 10.1016/j.nlm.2009.09.009pubmed: 19796703google scholar: lookup
  62. Balleine B.W., O’Doherty J.P.. Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action. Neuropsychopharmacology 2010;35:48–69.
    doi: 10.1038/npp.2009.131pmc: PMC3055420pubmed: 19776734google scholar: lookup
  63. Peeters M., Sulon J., Beckers J.-F., LeDoux D., Vandenheede M.. Comparison between blood serum and salivary cortisol concentrations in horses using an adrenocorticotropic hormone challenge. Equine Vet. J. 2011;43:487–493.
    doi: 10.1111/j.2042-3306.2010.00294.xpubmed: 21496072google scholar: lookup
  64. Barman S.M., Yates B.. Deciphering the Neural Control of Sympathetic Nerve Activity: Status Report and Directions for Future Research. Front. Neurosci. 2017;11:730.
    doi: 10.3389/fnins.2017.00730pmc: PMC5743742pubmed: 29311801google scholar: lookup
  65. Kurosawa M., Nagata S.-I., Takeda F., Mima K., Hiraga A., Kai M., Taya K.. Plasma Catecholamine, Adrenocorticotropin and Cortisol Responses to Exhaustive Incremental Treadmill Exercise of the Thoroughbred Horse. J. Equine Sci. 1998;9:9–18.
    doi: 10.1294/jes.9.9google scholar: lookup
  66. Baragli P., Pacchini S., Gatta D., Ducci M., Sighieri C.. Brief note about plasma catecholamines kinetics and submaximal exercise in untrained standardbreds. Ann. Dell’istituto Super. Di Sanità 2010;46:96–100.
    doi: 10.1590/s0021-25712010000100012pubmed: 20348624google scholar: lookup
  67. Hada T., Onaka T., Kusunose R., Yagi K.. Effects of Novel Environmental Stimuli on Neuroendocrine Activity in Thoroughbred Horses. J. Equine Sci. 2001;12:33–38.
    doi: 10.1294/jes.12.33google scholar: lookup
  68. Wascher C.A.F.. Heart rate as a measure of emotional arousal in evolutionary biology. Philos. Trans. R. Soc. B Biol. Sci. 2021;376:20200479.
    doi: 10.1098/rstb.2020.0479pmc: PMC8237168pubmed: 34176323google scholar: lookup
  69. Kongoun S., Chanda M., Piyachaturawat P., Saengsawang W.. Exercise increases brain-derived neurotrophic factor level in serum of horses. Livest. Sci. 2015;180:253–256.
    doi: 10.1016/j.livsci.2015.08.006google scholar: lookup
  70. Und T.B., Lessmann V.. BDNF: A regulator of learning and memory with clinical relevance. Neuroforum 2014;20:166–177.
  71. Halbach O.V.B.U., Halbach V.V.B.U.. BDNF effects on dendritic spine morphology and hippocampal function. Cell Tissue Res. 2018;373:729–741.
    doi: 10.1007/s00441-017-2782-xpubmed: 29450725google scholar: lookup
  72. Zagrebelsky M., Tacke C., Korte M.. BDNF signaling during the lifetime of dendritic spines. Cell Tissue Res. 2020;382:185–199.
    doi: 10.1007/s00441-020-03226-5pmc: PMC7529616pubmed: 32537724google scholar: lookup
  73. Bathina S., Das U.N.. Brain-derived neurotrophic factor and its clinical implications. Arch. Med. Sci. 2015;11:1164–1178.
    doi: 10.5114/aoms.2015.56342pmc: PMC4697050pubmed: 26788077google scholar: lookup
  74. Pluchino N., Russo M., Santoro A., Litta P., Cela V., Genazzani A.. Steroid hormones and BDNF. Neuroscience 2013;239:271–279.
    doi: 10.1016/j.neuroscience.2013.01.025pubmed: 23380505google scholar: lookup
  75. Jeanneteau F., Borie A., Chao M.V., Garabedian M.J.. Bridging the Gap between Brain-Derived Neurotrophic Factor and Glucocorticoid Effects on Brain Networks. Neuroendocrinology 2019;109:277–284.
    doi: 10.1159/000496392pubmed: 30572337google scholar: lookup
  76. Linz R., Puhlmann L.M.C., Apostolakou F., Mantzou E., Papassotiriou I., Chrousos G.P., Engert V., Singer T.. Acute psychosocial stress increases serum BDNF levels: An antagonistic relation to cortisol but no group differences after mental training. Neuropsychopharmacology 2019;44:1797–1804.
    doi: 10.1038/s41386-019-0391-ypmc: PMC6785147pubmed: 30991416google scholar: lookup
  77. Barfield E.T., Gerber K.J., Zimmermann K.S., Ressler K.J., Parsons R.G., Gourley S.L.. Regulation of actions and habits by ventral hippocampal trkB and adolescent corticosteroid exposure. PLoS Biol. 2017;15:e2003000.
    doi: 10.1371/journal.pbio.2003000pmc: PMC5724896pubmed: 29186135google scholar: lookup
  78. Klein A.B., Williamson R., Santini M.A., Clemmensen C., Ettrup A., Rios M., Knudsen G.M., Aznar S.. Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int. J. Neuropsychopharmacol. 2011;14:347–353.
    doi: 10.1017/S1461145710000738pubmed: 20604989google scholar: lookup
  79. Elfving B., Plougmann P.H., Wegener G.. Detection of brain-derived neurotrophic factor (BDNF) in rat blood and brain preparations using ELISA: Pitfalls and solutions. J. Neurosci. Methods 2010;187:73–77.
    doi: 10.1016/j.jneumeth.2009.12.017pubmed: 20043947google scholar: lookup
  80. Piepmeier A.T., Etnier J.L.. Brain-derived neurotrophic factor (BDNF) as a potential mechanism of the effects of acute exercise on cognitive performance. J. Sport Health Sci. 2015;4:14–23.
    doi: 10.1016/j.jshs.2014.11.001google scholar: lookup
  81. McGreevy P.D., McLean A.N.. Punishment in horse-training and the concept of ethical equitation. J. Vet. Behav. Clin. Appl. Res. 2009;4:193–197.
    doi: 10.1016/j.jveb.2008.08.001google scholar: lookup
  82. Schmidt A., Möstl E., Wehnert C., Aurich J., Müller J., Aurich C.. Cortisol release and heart rate variability in horses during road transport. Horm. Behav. 2010;57:209–215.
    doi: 10.1016/j.yhbeh.2009.11.003pubmed: 19944105google scholar: lookup
  83. Charmandari E., Tsigos C., Chrousos G.. Endocrinology of The Stress Response. Annu. Rev. Physiol. 2005;67:259–284.
    doi: 10.1146/annurev.physiol.67.040403.120816pubmed: 15709959google scholar: lookup
  84. Henshall C., Randle H., Francis N., Freire R.. The effect of stress and exercise on the learning performance of horses. Sci. Rep. 2022;12:1918.
    doi: 10.1038/s41598-021-03582-4pmc: PMC8816904pubmed: 35121736google scholar: lookup
  85. Tovote P., Fadok J.P., Lüthi A.. Neuronal circuits for fear and anxiety. Nat. Rev. Neurosci. 2015;16:317–331.
    doi: 10.1038/nrn3945pubmed: 25991441google scholar: lookup
  86. Deng H., Xiao X., Wang Z.. Periaqueductal Gray Neuronal Activities Underlie Different Aspects of Defensive Behaviors. J. Neurosci. 2016;36:7580–7588.
    doi: 10.1523/JNEUROSCI.4425-15.2016pmc: PMC6705556pubmed: 27445137google scholar: lookup
  87. Arnsten A.F.T.. Stress weakens prefrontal networks: Molecular insults to higher cognition. Nat. Neurosci. 2015;18:1376–1385.
    doi: 10.1038/nn.4087pmc: PMC4816215pubmed: 26404712google scholar: lookup
  88. Maier S.F., Seligman M.E.P.. Learned helplessness at fifty: Insights from neuroscience. Psychol. Rev. 2016;123:349–367.
    doi: 10.1037/rev0000033pmc: PMC4920136pubmed: 27337390google scholar: lookup
  89. Fernández-Teruel A., Tobeña A.. Revisiting the role of anxiety in the initial acquisition of two-way active avoidance: Pharmacological, behavioural and neuroanatomical convergence. Neurosci. Biobehav. Rev. 2020;118:739–758.
    doi: 10.1016/j.neubiorev.2020.08.014pubmed: 32916193google scholar: lookup
  90. Ahrendt L.P., Labouriau R., Malmkvist J., Nicol C., Christensen J.W.. Development of a standard test to assess negative reinforcement learning in horses. Appl. Anim. Behav. Sci. 2015;169:38–42.
    doi: 10.1016/j.applanim.2015.05.005google scholar: lookup
  91. Fenner K., Webb H., Starling M.J., Freire R., Buckley P., McGreevy P.. Effects of pre-conditioning on behavior and physiology of horses during a standardised learning task. PLoS ONE 2017;12:e0174313.
    doi: 10.1371/journal.pone.0174313pmc: PMC5373532pubmed: 28358892google scholar: lookup
  92. Byström A., Clayton H., Hernlund E., Rhodin M., Egenvall A.. Equestrian and biomechanical perspectives on laterality in the horse. Comp. Exerc. Physiol. 2020;16:35–45.
    doi: 10.3920/CEP190022google scholar: lookup
  93. Roozendaal B., Okuda S., Van der Zee E.A., McGaugh J.L.. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. USA 2006;103:6741–6746.
    doi: 10.1073/pnas.0601874103pmc: PMC1458951pubmed: 16611726google scholar: lookup
  94. Snow D.H., Harris R.C., Macdonald I.A., Forster C.D., Marlin D.J.. Effects of high-intensity exercise on plasma catecholamines in the Thoroughbred horse. Equine Vet. J. 1992;24:462–467.
    doi: 10.1111/j.2042-3306.1992.tb02877.xpubmed: 1459060google scholar: lookup
  95. Gruber A.J., McDonald R.J.. Context, emotion, and the strategic pursuit of goals: Interactions among multiple brain systems controlling motivated behavior. Front. Behav. Neurosci. 2012;6:50.
    doi: 10.3389/fnbeh.2012.00050pmc: PMC3411069pubmed: 22876225google scholar: lookup
  96. Schultz W.. Updating dopamine reward signals. Curr. Opin. Neurobiol. 2013;23:229–238.
    doi: 10.1016/j.conb.2012.11.012pmc: PMC3866681pubmed: 23267662google scholar: lookup
  97. Evans D.A., Stempel A.V., Vale R., Ruehle S., Lefler Y., Branco T.. A synaptic threshold mechanism for computing escape decisions. Nature 2018;558:590–594.
    doi: 10.1038/s41586-018-0244-6pmc: PMC6235113pubmed: 29925954google scholar: lookup
  98. de Jong J.W., Afjei S.A., Dorocic I.P., Peck J.R., Liu C., Kim C.K., Tian L., Deisseroth K., Lammel S.. A Neural Circuit Mechanism for Encoding Aversive Stimuli in the Mesolimbic Dopamine System. Neuron 2019;101:133–151.e7.
    doi: 10.1016/j.neuron.2018.11.005pmc: PMC6317997pubmed: 30503173google scholar: lookup
  99. Oleson E.B., Gentry R.N., Chioma V.C., Cheer J.. Subsecond Dopamine Release in the Nucleus Accumbens Predicts Conditioned Punishment and Its Successful Avoidance. J. Neurosci. 2012;32:14804–14808.
    doi: 10.1523/JNEUROSCI.3087-12.2012pmc: PMC3498047pubmed: 23077064google scholar: lookup
  100. Gentry R.N., Schuweiler D.R., Roesch M.R.. Dopamine signals related to appetitive and aversive events in paradigms that manipulate reward and avoidability. Brain Res. 2019;1713:80–90.
    doi: 10.1016/j.brainres.2018.10.008pmc: PMC6826219pubmed: 30300635google scholar: lookup
  101. Stelly C.E., Haug G.C., Fonzi K.M., Garcia M.A., Tritley S.C., Magnon A.P., Ramos M.A.P., Wanat M.J.. Pattern of dopamine signaling during aversive events predicts active avoidance learning. Proc. Natl. Acad. Sci. USA 2019;116:13641–13650.
    doi: 10.1073/pnas.1904249116pmc: PMC6613186pubmed: 31209016google scholar: lookup
  102. Pultorak K.J., Schelp S., Isaacs D.P., Krzystyniak G., Oleson E.B.. A Transient Dopamine Signal Represents Avoidance Value and Causally Influences the Demand to Avoid. Eneuro 2018:1–18.
    doi: 10.1523/ENEURO.0058-18.2018pmc: PMC5952648pubmed: 29766047google scholar: lookup
  103. Wendler E., Gaspar J.C., Ferreira T.L., Barbiero J.K., Andreatini R., Vital M.A., Blaha C.D., Winn P., Da Cunha C.. The roles of the nucleus accumbens core, dorsomedial striatum, and dorsolateral striatum in learning: Performance and extinction of Pavlovian fear-conditioned responses and instrumental avoidance responses. Neurobiol. Learn. Mem. 2014;109:27–36.
    doi: 10.1016/j.nlm.2013.11.009pubmed: 24291572google scholar: lookup
  104. Hulme S.R., Jones O.D., Abraham W.C.. Emerging roles of metaplasticity in behaviour and disease. Trends Neurosci. 2013;36:353–362.
    doi: 10.1016/j.tins.2013.03.007pubmed: 23602195google scholar: lookup
  105. Parsons R.G.. Behavioral and neural mechanisms by which prior experience impacts subsequent learning. Neurobiol. Learn. Mem. 2018;154:22–29.
    doi: 10.1016/j.nlm.2017.11.008pubmed: 29155095google scholar: lookup
  106. Bailey C.H., Kandel E.R., Harris K.. Structural Components of Synaptic Plasticity and Memory Consolidation. Cold Spring Harb. Perspect. Biol. 2015;7:a021758.
    doi: 10.1101/cshperspect.a021758pmc: PMC4484970pubmed: 26134321google scholar: lookup
  107. Joëls M., Pasricha N., Karst H.. The interplay between rapid and slow corticosteroid actions in brain. Eur. J. Pharmacol. 2013;719:44–52.
    doi: 10.1016/j.ejphar.2013.07.015pubmed: 23886619google scholar: lookup
  108. Q껟lieg C.W.E.M., Schwabe L.. Memory dynamics under stress. Memory 2018;26:364–376.
    doi: 10.1080/09658211.2017.1338299pubmed: 28625108google scholar: lookup
  109. Conrad C.D.. A critical review of chronic stress effects on spatial learning and memory. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2010;34:742–755.
    doi: 10.1016/j.pnpbp.2009.11.003pubmed: 19903505google scholar: lookup
  110. Dias-Ferreira E., Sousa J.C., Melo I., Morgado P., Mesquita A.R., Cerqueira J.J., Costa R.M., Sousa N.. Chronic Stress Causes Frontostriatal Reorganization and Affects Decision-Making. Science 2009;325:621–625.
    doi: 10.1126/science.1171203pubmed: 19644122google scholar: lookup
  111. Taylor S., Anglin J., Paode P., Riggert A., Olive F., Conrad C.. Chronic stress may facilitate the recruitment of habit- and addiction-related neurocircuitries through neuronal restructuring of the striatum. Neuroscience 2014;280:231–242.
    doi: 10.1016/j.neuroscience.2014.09.029pmc: PMC4256944pubmed: 25242641google scholar: lookup
  112. Cockrem J.F.. Individual variation in glucocorticoid stress responses in animals. Gen. Comp. Endocrinol. 2013;181:45–58.
    doi: 10.1016/j.ygcen.2012.11.025pubmed: 23298571google scholar: lookup
  113. Díaz-Morán S., Palència M., Mont-Cardona C., Cañete T., Blázquez G., Martínez-Membrives E., López-Aumatell R., Tobeña A., Fernández-Teruel A.. Coping style and stress hormone responses in genetically heterogeneous rats: Comparison with the Roman rat strains. Behav. Brain Res. 2012;228:203–210.
    doi: 10.1016/j.bbr.2011.12.002pubmed: 22178313google scholar: lookup
  114. Smeets T., van Ruitenbeek P., Hartogsveld B., Q껟lieg C.W.. Stress-induced reliance on habitual behavior is moderated by cortisol reactivity. Brain Cogn. 2019;133:60–71.
    doi: 10.1016/j.bandc.2018.05.005pubmed: 29807661google scholar: lookup
  115. Sauer F.J., Hermann M., Ramseyer A., Burger D., Riemer S., Gerber V.. Effects of breed, management and personality on cortisol reactivity in sport horses. PLoS ONE 2019;14:e0221794.
    doi: 10.1371/journal.pone.0221794pmc: PMC6886778pubmed: 31790402google scholar: lookup
  116. 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 2017;12:e0170783.
    doi: 10.1371/journal.pone.0170783pmc: PMC5419560pubmed: 28475581google scholar: lookup
  117. Valenchon M., Lévy F., Prunier A., Moussu C., Calandreau L., Lansade L.. Stress Modulates Instrumental Learning Performances in Horses (Equus caballus) in Interaction with Temperament. PLoS ONE 2013;8:e62324.
    doi: 10.1371/journal.pone.0062324pmc: PMC3633893pubmed: 23626801google scholar: lookup
  118. Lakshminarasimhan H., Chattarji S.. Stress Leads to Contrasting Effects on the Levels of Brain Derived Neurotrophic Factor in the Hippocampus and Amygdala. PLoS ONE 2012;7:e30481.
    doi: 10.1371/journal.pone.0030481pmc: PMC3260293pubmed: 22272355google scholar: lookup
  119. Bennett M., Lagopoulos J.. Stress and trauma: BDNF control of dendritic-spine formation and regression. Prog. Neurobiol. 2014;112:80–99.
    doi: 10.1016/j.pneurobio.2013.10.005pubmed: 24211850google scholar: lookup
  120. Jeanneteau F., Chao M.. Are BDNF and glucocorticoid activities calibrated?. Neuroscience 2013;239:173–195.
    doi: 10.1016/j.neuroscience.2012.09.017pmc: PMC3581703pubmed: 23022538google scholar: lookup
  121. Rasmussen P., Brassard P., Adser H., Pedersen M.V., Leick L., Hart E., Secher N.H., Pedersen B.K., Pilegaard H.. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp. Physiol. 2009;94:1062–1069.
    doi: 10.1113/expphysiol.2009.048512pubmed: 19666694google scholar: lookup
  122. Walsh J.J., Tschakovsky M.E.. Exercise and circulating BDNF: Mechanisms of release and implications for the design of exercise interventions. Appl. Physiol. Nutr. Metab. 2018;43:1095–1104.
    doi: 10.1139/apnm-2018-0192pubmed: 29775542google scholar: lookup
  123. Conrad C.D., Ortiz J.B., Judd J.M.. Chronic stress and hippocampal dendritic complexity: Methodological and functional considerations. Physiol. Behav. 2017;178:66–81.
    doi: 10.1016/j.physbeh.2016.11.017pubmed: 27887995google scholar: lookup
  124. Vyas A., Mitra R., Rao B.S.S., Chattarji S.. Chronic Stress Induces Contrasting Patterns of Dendritic Remodeling in Hippocampal and Amygdaloid Neurons. J. Neurosci. 2002;22:6810–6818.
    doi: 10.1523/JNEUROSCI.22-15-06810.2002pmc: PMC6758130pubmed: 12151561google scholar: lookup
  125. Maroun M., Ioannides P.J., Bergman K.L., Kavushansky A., Holmes A., Wellman C.L.. Fear extinction deficits following acute stress associate with increased spine density and dendritic retraction in basolateral amygdala neurons. Eur. J. Neurosci. 2013;38:2611–2620.
    doi: 10.1111/ejn.12259pmc: PMC3773716pubmed: 23714419google scholar: lookup

Citations

This article has been cited 2 times.
  1. Wonghanchao T, Huangsaksri O, Sanigavatee K, Poochipakorn C, Chanprame S, Wongkosoljit S, Chotiyothin W, Rattanayanon N, Kiawwan R, Chanda M. Autonomic regulation in athletic horses repetitively participating in two novice jumping classes on consecutive days. Front Vet Sci 2024;11:1456733.
    doi: 10.3389/fvets.2024.1456733pubmed: 39502949google scholar: lookup
  2. Pereira-Figueiredo I, Rosa I, Sancho Sanchez C. Forced Handling Decreases Emotionality but Does Not Improve Young Horses' Responses toward Humans and their Adaptability to Stress. Animals (Basel) 2024 Mar 2;14(5).
    doi: 10.3390/ani14050784pubmed: 38473169google scholar: lookup
Subscribe to our newsletter
Join 99,911 horse owners like you who receive our email updates on horse health and nutrition.