Analyze Diet
Scientific reports2019; 9(1); 11568; doi: 10.1038/s41598-019-47960-5

Horses associate individual human voices with the valence of past interactions: a behavioural and electrophysiological study.

Abstract: Brain lateralization is a phenomenon widely reported in the animal kingdom and sensory laterality has been shown to be an indicator of the appraisal of the stimulus valence by an individual. This can prove a useful tool to investigate how animals perceive intra- or hetero-specific signals. The human-animal relationship provides an interesting framework for testing the impact of the valence of interactions on emotional memories. In the present study, we tested whether horses could associate individual human voices with past positive or negative experiences. Both behavioural and electroencephalographic measures allowed examining laterality patterns in addition to the behavioural reactions. The results show that horses reacted to voices associated with past positive experiences with increased attention/arousal (gamma oscillations in the right hemisphere) and indicators of a positive emotional state (left hemisphere activation and ears held forward), and to those associated with past negative experiences with negative affective states (right hemisphere activation and ears held backwards). The responses were further influenced by the animals' management conditions (e.g. box or pasture). Overall, these results, associating brain and behaviour analysis, clearly demonstrate that horses' representation of human voices is modulated by the valence of prior horse-human interactions.
Publication Date: 2019-08-09 PubMed ID: 31399629PubMed Central: PMC6689011DOI: 10.1038/s41598-019-47960-5Google 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.

The research explores the ability of horses to associate individual human voices with previous positive or negative experiences, with a focus on the animals’ behavioural and brain responses.

Objective of the study

The research aimed to study ‘brain lateralization’ in horses and how it affects their response to human voices based on their past experiences.

  • Brain lateralization refers to the fact that the left and right hemispheres of the brain are not identical and have different functions, seen in different species across the animal kingdom.
  • This phenomenon is particularly relevant to how animals perceive and respond to intra-species or inter-species signals, for instance, human voices in the case of horses.

Methodology of the study

The researchers conducted behavioural tests and electroencephalographic (EEG) measures on horses, associating human voices with either positive or negative past experiences.

  • The behavioural tests were designed to observe horses’ immediate reactions to the voices.
  • The EEG measures were used to explore the patterns of brain activity and lateralization occurring in response to the voices. This was done by measuring gamma oscillations and noting which hemisphere of the brain was more activated.

Results of the study

The findings revealed that horses could indeed associate human voices with prior positive or negative experiences, and react accordingly.

  • Horses responded to human voices linked to past positive experiences with increased attention or arousal. This was particularly represented by increased gamma oscillations in the right hemisphere and signs of a positive emotional state – activation of the left hemisphere and forward-held ears.
  • Conversely, horses linked voices from past negative experiences with negative emotional states – this was evidenced by the activation of the right hemisphere and their ears held backward.
  • The researchers found that the horses’ responses were further influenced by their management conditions, such as whether they were kept in a box or pasture.

Conclusions of the study

The study concludes that horses’ perceptions of human voices are modulated by the nature (positive or negative) of their prior interactions with humans. This was demonstrated by the physical behaviours of horses and their brain responses to human voices, a finding that establishes a significant bridge between behaviour and brain analysis in the study of animal emotions.

Cite This Article

APA
(2019). Horses associate individual human voices with the valence of past interactions: a behavioural and electrophysiological study. Sci Rep, 9(1), 11568. https://doi.org/10.1038/s41598-019-47960-5

Publication

ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 9
Issue: 1
Pages: 11568
PII: 11568

Researcher Affiliations

MeSH Terms

  • Animals
  • Attention
  • Behavior, Animal
  • Brain / physiology
  • Electroencephalography
  • Emotions
  • Functional Laterality
  • Horses / physiology
  • Human-Animal Bond
  • Humans
  • Voice

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 68 references
  1. Rogers LJ, Vallortigara G, Andrew RJ. Divided brains: the biology and behaviour of brain asymmetries. .
  2. Vallortigara G, Chiandetti C, Sovrano VA. Brain asymmetry (animal).. Wiley Interdiscip Rev Cogn Sci 2011 Mar;2(2):146-157.
    doi: 10.1002/wcs.100pubmed: 26302006google scholar: lookup
  3. Poremba A, Malloy M, Saunders RC, Carson RE, Herscovitch P, Mishkin M. Species-specific calls evoke asymmetric activity in the monkey's temporal poles.. Nature 2004 Jan 29;427(6973):448-51.
    doi: 10.1038/nature02268pubmed: 14749833google scholar: lookup
  4. Ghazanfar AA, Hauser MD. The auditory behaviour of primates: a neuroethological perspective.. Curr Opin Neurobiol 2001 Dec;11(6):712-20.
    doi: 10.1016/S0959-4388(01)00274-4pubmed: 11741023google scholar: lookup
  5. Baciadonna L, Nawroth C, Briefer EF, McElligott AG. Perceptual lateralization of vocal stimuli in goats.. Curr Zool 2019 Feb;65(1):67-74.
    doi: 10.1093/cz/zoy022pmc: PMC6347058pubmed: 30697240google scholar: lookup
  6. Böye M, Güntürkün O, Vauclair J. Right ear advantage for conspecific calls in adults and subadults, but not infants, California sea lions (Zalophus californianus): hemispheric specialization for communication?. Eur J Neurosci 2005 Mar;21(6):1727-32.
  7. Palleroni A, Hauser M. Experience-dependent plasticity for auditory processing in a raptor.. Science 2003 Feb 21;299(5610):1195.
    doi: 10.1126/science.1078813pubmed: 12595683google scholar: lookup
  8. Siniscalchi M, Laddago S, Quaranta A. Auditory lateralization of conspecific and heterospecific vocalizations in cats.. Laterality 2016;21(3):215-27.
    doi: 10.1080/1357650X.2015.1116541pubmed: 26618245google scholar: lookup
  9. Siniscalchi M, Quaranta A, Rogers LJ. Hemispheric specialization in dogs for processing different acoustic stimuli.. PLoS One 2008;3(10):e3349.
  10. Gil-da-Costa R, Hauser MD. Vervet monkeys and humans show brain asymmetries for processing conspecific vocalizations, but with opposite patterns of laterality.. Proc Biol Sci 2006 Sep 22;273(1599):2313-8.
    doi: 10.1098/rspb.2006.3580pmc: PMC1636091pubmed: 16928633google scholar: lookup
  11. Lemasson A, Koda H, Kato A, Oyakawa C, Blois-Heulin C, Masataka N. Influence of sound specificity and familiarity on Japanese macaques' (Macaca fuscata) auditory laterality.. Behav Brain Res 2010 Mar 17;208(1):286-9.
    doi: 10.1016/j.bbr.2009.12.008pubmed: 20006649google scholar: lookup
  12. George I, Vernier B, Richard JP, Hausberger M, Cousillas H. Hemispheric specialization in the primary auditory area of awake and anesthetized starlings (Sturnus vulgaris).. Behav Neurosci 2004 Jun;118(3):597-610.
    doi: 10.1037/0735-7044.118.3.597pubmed: 15174938google scholar: lookup
  13. George I, Cousillas H, Richard JP, Hausberger M. State-dependent hemispheric specialization in the songbird brain.. J Comp Neurol 2005 Jul 18;488(1):48-60.
    doi: 10.1002/cne.20584pubmed: 15912499google scholar: lookup
  14. Scheumann M, Zimmermann E. Do mouse lemurs show asymmetries in handedness and the perception of communication calls?. Primate Rep 2005;72:84–85.
  15. Teufel C, Hammerschmidt K, Fischer J. Lack of orienting asymmetries in Barbary macaques: implications for studies of lateralized auditory processing. Anim. Behav. 2007;73:249–255.
  16. Cynx J, Williams H, Nottebohm F. Hemispheric differences in avian song discrimination.. Proc Natl Acad Sci U S A 1992 Feb 15;89(4):1372-5.
    doi: 10.1073/pnas.89.4.1372pmc: PMC48452pubmed: 1741391google scholar: lookup
  17. Hausberger M. A Crucial Role of Attention in Lateralisation of Sound Processing?. Symmetry 2019;11:48.
    doi: 10.3390/sym11010048google scholar: lookup
  18. Demaree HA, Everhart DE, Youngstrom EA, Harrison DW. Brain lateralization of emotional processing: historical roots and a future incorporating "dominance".. Behav Cogn Neurosci Rev 2005 Mar;4(1):3-20.
    doi: 10.1177/1534582305276837pubmed: 15886400google scholar: lookup
  19. Basile M, Lemasson A, Blois-Heulin C. Social and emotional values of sounds influence human (Homo sapiens) and non-human primate (Cercopithecus campbelli) auditory laterality.. PLoS One 2009 Jul 17;4(7):e6295.
  20. Hauser MD, Andersson K. Left hemisphere dominance for processing vocalizations in adult, but not infant, rhesus monkeys: field experiments.. Proc Natl Acad Sci U S A 1994 Apr 26;91(9):3946-8.
    doi: 10.1073/pnas.91.9.3946pmc: PMC43699pubmed: 8171017google scholar: lookup
  21. Siniscalchi M, d'Ingeo S, Fornelli S, Quaranta A. Lateralized behavior and cardiac activity of dogs in response to human emotional vocalizations.. Sci Rep 2018 Jan 8;8(1):77.
    doi: 10.1038/s41598-017-18417-4pmc: PMC5758824pubmed: 29311574google scholar: lookup
  22. Smith AV, Proops L, Grounds K, Wathan J, Scott SK, McComb K. Domestic horses (Equus caballus) discriminate between negative and positive human nonverbal vocalisations.. Sci Rep 2018 Aug 29;8(1):13052.
    doi: 10.1038/s41598-018-30777-zpmc: PMC6115467pubmed: 30158532google scholar: lookup
  23. Rogers LJ. Relevance of brain and behavioural lateralization to animal welfare. Appl. Anim. Behav. Sci. 2010;127:1–11.
  24. Siniscalchi M, Bertino D, d’Ingeo S, Quaranta A. Relationship between motor laterality and aggressive behavior in sheepdogs. Symmetry 2019;11:233.
    doi: 10.3390/sym11020233google scholar: lookup
  25. Siniscalchi M, d'Ingeo S, Quaranta A. Orienting asymmetries and physiological reactivity in dogs' response to human emotional faces.. Learn Behav 2018 Dec;46(4):574-585.
    doi: 10.3758/s13420-018-0325-2pubmed: 29923158google scholar: lookup
  26. Andics A, Gácsi M, Faragó T, Kis A, Miklósi A. Voice-sensitive regions in the dog and human brain are revealed by comparative fMRI.. Curr Biol 2014 Mar 3;24(5):574-8.
    doi: 10.1016/j.cub.2014.01.058pubmed: 24560578google scholar: lookup
  27. Rochais C, Sébilleau M, Menoret M, Oger M, Henry S, Hausberger M, Cousillas H. Attentional state and brain processes: state-dependent lateralization of EEG profiles in horses.. Sci Rep 2018 Jul 5;8(1):10153.
    doi: 10.1038/s41598-018-28334-9pmc: PMC6033862pubmed: 29976936google scholar: lookup
  28. Balconi M, Vanutelli ME. Vocal and visual stimulation, congruence and lateralization affect brain oscillations in interspecies emotional positive and negative interactions.. Soc Neurosci 2016;11(3):297-310.
    doi: 10.1080/17470919.2015.1081400pubmed: 26256040google scholar: lookup
  29. Teufel C, Ghazanfar AA, Fischer J. On the relationship between lateralized brain function and orienting asymmetries.. Behav Neurosci 2010 Aug;124(4):437-45.
    doi: 10.1037/a0019925pubmed: 20695643google scholar: lookup
  30. Basile M, Boivin S, Boutin A, Blois-Heulin C, Hausberger M, Lemasson A. Socially dependent auditory laterality in domestic horses (Equus caballus).. Anim Cogn 2009 Jul;12(4):611-9.
    doi: 10.1007/s10071-009-0220-5pubmed: 19283416google scholar: lookup
  31. Ocklenburg S, Ströckens F, Güntürkün O. Lateralisation of conspecific vocalisation in non-human vertebrates.. Laterality 2013;18(1):1-31.
    doi: 10.1080/1357650X.2011.626561pubmed: 23231542google scholar: lookup
  32. Rogers LJ. Eye and Ear Preferences. In Lateralized Brain Functions- Methods in Human and Non-Human Species, 79–102 (Humana Press, 2017).
  33. Ratcliffe VF, Reby D. Orienting asymmetries in dogs' responses to different communicatory components of human speech.. Curr Biol 2014 Dec 15;24(24):2908-12.
    doi: 10.1016/j.cub.2014.10.030pubmed: 25454584google scholar: lookup
  34. Andics A, Gábor A, Gácsi M, Faragó T, Szabó D, Miklósi Á. Neural mechanisms for lexical processing in dogs.. Science 2016 Sep 2;353(6303):1030-1032.
    doi: 10.1126/science.aaf3777pubmed: 27576923google scholar: lookup
  35. Leblanc MA. The mind of the horse: An introduction to equine cognition. .
  36. Tallet C, Rakotomahandry M, Guérin C, Lemasson A, Hausberger M. Postnatal auditory preferences in piglets differ according to maternal emotional experience with the same sounds during gestation.. Sci Rep 2016 Nov 18;6:37238.
    doi: 10.1038/srep37238pmc: PMC5114567pubmed: 27857224google scholar: lookup
  37. Saito A, Shinozuka K. Vocal recognition of owners by domestic cats (Felis catus).. Anim Cogn 2013 Jul;16(4):685-90.
    doi: 10.1007/s10071-013-0620-4pubmed: 23525707google scholar: lookup
  38. Thieltges H, Lemasson A, Kuczaj S, Böye M, Blois-Heulin C. Visual laterality in dolphins when looking at (un)familiar humans.. Anim Cogn 2011 Mar;14(2):303-8.
    doi: 10.1007/s10071-010-0354-5pubmed: 21140186google scholar: lookup
  39. Yeater DB, Hill HM, Baus N, Farnell H, Kuczaj SA 2nd. Visual laterality in belugas (Delphinapterus leucas) and Pacific white-sided dolphins (Lagenorhynchus obliquidens) when viewing familiar and unfamiliar humans.. Anim Cogn 2014 Nov;17(6):1245-59.
    doi: 10.1007/s10071-014-0756-xpubmed: 24831888google scholar: lookup
  40. Peirce JW, Leigh AE, daCosta AP, Kendrick KM. Human face recognition in sheep: lack of configurational coding and right hemisphere advantage.. Behav Processes 2001 Jun 13;55(1):13-26.
    doi: 10.1016/S0376-6357(01)00158-9pubmed: 11390088google scholar: lookup
  41. Sankey C, Henry S, André N, Richard-Yris MA, Hausberger M. Do horses have a concept of person?. PLoS One 2011 Mar 30;6(3):e18331.
  42. Krueger K, Flauger B, Farmer K, Maros K. Horses (Equus caballus) use human local enhancement cues and adjust to human attention.. Anim Cogn 2011 Mar;14(2):187-201.
    doi: 10.1007/s10071-010-0352-7pubmed: 20845052google scholar: lookup
  43. Lampe JF, Andre J. Cross-modal recognition of human individuals in domestic horses (Equus caballus).. Anim Cogn 2012 Jul;15(4):623-30.
    doi: 10.1007/s10071-012-0490-1pubmed: 22526687google scholar: lookup
  44. Proops L, McComb K. Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans.. Proc Biol Sci 2012 Aug 22;279(1741):3131-8.
    pmc: PMC3385734pubmed: 22593108doi: 10.1098/rspb.2012.0626google scholar: lookup
  45. Fureix C, Jego P, Sankey C, Hausberger M. How horses (Equus caballus) see the world: humans as significant "objects".. Anim Cogn 2009 Jul;12(4):643-54.
    doi: 10.1007/s10071-009-0223-2pubmed: 19381698google scholar: lookup
  46. Hausberger M, Roche H, Henry S, Visser EK. A review of the human–horse relationship. Appl. Anim. Behav. Sci. 2008;109:1–24.
  47. Sankey C, Richard-Yris MA, Leroy H, Henry S, Hausberger M. Positive interactions lead to lasting positive memories in horses, Equus caballus. Anim. Behav. 2010;79:869–875.
  48. Sankey C, Richard-Yris MA, Henry S, Fureix C, Nassur F, Hausberger M. Reinforcement as a mediator of the perception of humans by horses (Equus caballus).. Anim Cogn 2010 Sep;13(5):753-64.
    doi: 10.1007/s10071-010-0326-9pubmed: 20490592google scholar: lookup
  49. Hausberger M, Muller C. A brief note on some possible factors involved in the reactions of horses to humans. Appl. Anim. Behav. Sci. 2002;76:339–344.
  50. Henry S, Fureix C, Rowberry R, Bateson M, Hausberger M. Do horses with poor welfare show 'pessimistic' cognitive biases?. Naturwissenschaften 2017 Feb;104(1-2):8.
    doi: 10.1007/s00114-016-1429-1pubmed: 28083632google scholar: lookup
  51. Lesimple C, Fureix C, LeScolan N, Richard-Yris MA, Hausberger M. Housing conditions and breed are associated with emotionality and cognitive abilities in riding school horses. Appl. Anim. Behav. Sci. 2011;129:92–99.
  52. Burn CC, Dennison TL, Whay HR. Relationships between behaviour and health in working horses, donkeys, and mules in developing countries. Appl. Anim. Behav. Sci. 2010;126:109–118.
  53. Waring GH. Horse behavior. .
  54. Fitzgibbon SP, Pope KJ, Mackenzie L, Clark CR, Willoughby JO. Cognitive tasks augment gamma EEG power.. Clin Neurophysiol 2004 Aug;115(8):1802-9.
    doi: 10.1016/j.clinph.2004.03.009pubmed: 15261859google scholar: lookup
  55. Harman AM, Moore S, Hoskins R, Keller P. Horse vision and an explanation for the visual behaviour originally explained by the 'ramp retina'.. Equine Vet J 1999 Sep;31(5):384-90.
  56. Siniscalchi M, d’Ingeo S, Quaranta A. Lateralized Functions in the Dog Brain. Symmetry 2017;9:71.
    doi: 10.3390/sym9050071google scholar: lookup
  57. Larose C, Richard-Yris MA, Hausberger M, Rogers LJ. Laterality of horses associated with emotionality in novel situations.. Laterality 2006 Jul;11(4):355-67.
    doi: 10.1080/13576500600624221pubmed: 16754236google scholar: lookup
  58. Sankey C, Henry S, Clouard C, Richard-Yris MA, Hausberger M. Asymmetry of behavioral responses to a human approach in young naive vs. trained horses.. Physiol Behav 2011 Sep 1;104(3):464-8.
    doi: 10.1016/j.physbeh.2011.05.009pubmed: 21605580google scholar: lookup
  59. De Boyer Des Roches A, Richard-Yris MA, Henry S, Ezzaouïa M, Hausberger M. Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects' emotional value.. Physiol Behav 2008 Jun 9;94(3):487-90.
    doi: 10.1016/j.physbeh.2008.03.002pubmed: 18455205google scholar: lookup
  60. Siegel M, Warden MR, Miller EK. Phase-dependent neuronal coding of objects in short-term memory.. Proc Natl Acad Sci U S A 2009 Dec 15;106(50):21341-6.
    doi: 10.1073/pnas.0908193106pmc: PMC2779828pubmed: 19926847google scholar: lookup
  61. Düzel E, Penny WD, Burgess N. Brain oscillations and memory.. Curr Opin Neurobiol 2010 Apr;20(2):143-9.
    doi: 10.1016/j.conb.2010.01.004pubmed: 20181475google scholar: lookup
  62. Knyazev GG. Motivation, emotion, and their inhibitory control mirrored in brain oscillations.. Neurosci Biobehav Rev 2007;31(3):377-95.
  63. Jensen O, Kaiser J, Lachaux JP. Human gamma-frequency oscillations associated with attention and memory.. Trends Neurosci 2007 Jul;30(7):317-24.
    doi: 10.1016/j.tins.2007.05.001pubmed: 17499860google scholar: lookup
  64. Rochais C, Henry S, Sankey C, Nassur F, Góracka-Bruzda A, Hausberger M. Visual attention, an indicator of human-animal relationships? A study of domestic horses (Equus caballus).. Front Psychol 2014;5:108.
    doi: 10.3389/fpsyg.2014.00108pmc: PMC3923161pubmed: 24592244google scholar: lookup
  65. Lesimple C, Poissonnet A, Hausberger M. How to keep your horse safe? An epidemiological study about management practices. Appl. Anim. Behav. Sci. 2016;181:105–114.
  66. Lesimple C, Fureix C, Menguy H, Hausberger M. Human direct actions may alter animal welfare, a study on horses (Equus caballus).. PLoS One 2010 Apr 28;5(4):e10257.
  67. 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 Vet Sci 2017;4:57.
    doi: 10.3389/fvets.2017.00057pmc: PMC5411420pubmed: 28512633google scholar: lookup
  68. Ishii R, Canuet L, Ishihara T, Aoki Y, Ikeda S, Hata M, Katsimichas T, Gunji A, Takahashi H, Nakahachi T, Iwase M, Takeda M. Frontal midline theta rhythm and gamma power changes during focused attention on mental calculation: an MEG beamformer analysis.. Front Hum Neurosci 2014;8:406.
    doi: 10.3389/fnhum.2014.00406pmc: PMC4052629pubmed: 24966825google scholar: lookup

Citations

This article has been cited 26 times.
  1. Rogers LJ. Knowledge of lateralized brain function can contribute to animal welfare. Front Vet Sci 2023;10:1242906.
    doi: 10.3389/fvets.2023.1242906pubmed: 37601762google scholar: lookup
  2. Krueger K, Gruentjens T, Hempel E. Wolf contact in horses at permanent pasture in Germany. PLoS One 2023;18(8):e0289767.
    doi: 10.1371/journal.pone.0289767pubmed: 37561797google scholar: lookup
  3. Felici M, Reddon AR, Maglieri V, Lanatà A, Baragli P. Heart and brain: Change in cardiac entropy is related to lateralised visual inspection in horses. PLoS One 2023;18(8):e0289753.
    doi: 10.1371/journal.pone.0289753pubmed: 37552685google scholar: lookup
  4. d'Ingeo S, Siniscalchi M, Straziota V, Ventriglia G, Sasso R, Quaranta A. Relationship between asymmetric nostril use and human emotional odours in cats. Sci Rep 2023 Jul 6;13(1):10982.
    doi: 10.1038/s41598-023-38167-wpubmed: 37414814google scholar: lookup
  5. Jardat P, Destrez A, Damon F, Menard-Peroy Z, Parias C, Barrière P, Keller M, Calandreau L, Lansade L. Horses discriminate human body odors between fear and joy contexts in a habituation-discrimination protocol. Sci Rep 2023 Feb 25;13(1):3285.
    doi: 10.1038/s41598-023-30119-8pubmed: 36841856google scholar: lookup
  6. Wijnen B, Martens P. Animals in Animal-Assisted Services: Are They Volunteers or Professionals?. Animals (Basel) 2022 Sep 26;12(19).
    doi: 10.3390/ani12192564pubmed: 36230304google scholar: lookup
  7. Wiśniewska A, Janczarek I, Ryżak M, Tkaczyk E, Kędzierski W. Behavioural responses of Konik Polski horses to natural, familiar sound of thunderstorm, and unfamiliar similar-sounding sounds of volcanic eruption and sea storms. BMC Vet Res 2022 May 30;18(1):207.
    doi: 10.1186/s12917-022-03314-4pubmed: 35637528google scholar: lookup
  8. Krueger K, Schwarz S, Marr I, Farmer K. Laterality in Horse Training: Psychological and Physical Balance and Coordination and Strength Rather Than Straightness. Animals (Basel) 2022 Apr 16;12(8).
    doi: 10.3390/ani12081042pubmed: 35454288google scholar: lookup
  9. Coria-Avila GA, Pfaus JG, Orihuela A, Domínguez-Oliva A, José-Pérez N, Hernández LA, Mota-Rojas D. The Neurobiology of Behavior and Its Applicability for Animal Welfare: A Review. Animals (Basel) 2022 Apr 4;12(7).
    doi: 10.3390/ani12070928pubmed: 35405916google scholar: lookup
  10. Bálint A, Eleőd H, Magyari L, Kis A, Gácsi M. Differences in dogs' event-related potentials in response to human and dog vocal stimuli; a non-invasive study. R Soc Open Sci 2022 Apr;9(4):211769.
    doi: 10.1098/rsos.211769pubmed: 35401994google scholar: lookup
  11. Krueger K, Esch L, Byrne R. Need or opportunity? A study of innovations in equids. PLoS One 2021;16(9):e0257730.
    doi: 10.1371/journal.pone.0257730pubmed: 34570831google scholar: lookup
  12. Jardat P, Lansade L. Cognition and the human-animal relationship: a review of the sociocognitive skills of domestic mammals toward humans. Anim Cogn 2022 Apr;25(2):369-384.
    doi: 10.1007/s10071-021-01557-6pubmed: 34476652google scholar: lookup
  13. d'Angelo D, d'Ingeo S, Ciani F, Visone M, Sacchettino L, Avallone L, Quaranta A. Cortisol Levels of Shelter Dogs in Animal Assisted Interventions in a Prison: An Exploratory Study. Animals (Basel) 2021 Jan 29;11(2).
    doi: 10.3390/ani11020345pubmed: 33572936google scholar: lookup
  14. Scopa C, Greco A, Contalbrigo L, Fratini E, Lanatà A, Scilingo EP, Baragli P. Inside the Interaction: Contact With Familiar Humans Modulates Heart Rate Variability in Horses. Front Vet Sci 2020;7:582759.
    doi: 10.3389/fvets.2020.582759pubmed: 33330706google scholar: lookup
  15. Quaranta A, d'Ingeo S, Amoruso R, Siniscalchi M. Emotion Recognition in Cats. Animals (Basel) 2020 Jun 28;10(7).
    doi: 10.3390/ani10071107pubmed: 32605256google scholar: lookup
  16. Contreras-Aguilar MD, Henry S, Coste C, Tecles F, Escribano D, Cerón JJ, Hausberger M. Changes in Saliva Analytes Correlate with Horses' Behavioural Reactions to An Acute Stressor: A Pilot Study. Animals (Basel) 2019 Nov 18;9(11).
    doi: 10.3390/ani9110993pubmed: 31752194google scholar: lookup
  17. Bernauer K, Kollross H, Schuetz A, Farmer K, Krueger K. How do horses (Equus caballus) learn from observing human action?. Anim Cogn 2020 Jan;23(1):1-9.
    doi: 10.1007/s10071-019-01310-0pubmed: 31531748google scholar: lookup
  18. Jardat P, Destrez A, Damon F, Tanguy-Guillo N, Lainé AL, Parias C, Reigner F, Ferreira VHB, Calandreau L, Lansade L. Human emotional odours influence horses' behaviour and physiology. PLoS One 2026;21(1):e0337948.
    doi: 10.1371/journal.pone.0337948pubmed: 41533708google scholar: lookup
  19. Ricci-Bonot C, Brosche K, Baragli P, Nicol C. A systematic review on the effect of individual characteristics and management practices on equine cognition. Anim Cogn 2025 Nov 26;28(1):96.
    doi: 10.1007/s10071-025-02016-2pubmed: 41296132google scholar: lookup
  20. Larrigaldie I, Damon F, Brimaud D, Lansade L, Schaal B, Destrez A. Behaviour of ewes and lambs in response to human emotional odours. Sci Rep 2025 Nov 24;15(1):45234.
    doi: 10.1038/s41598-025-29186-wpubmed: 41286085google scholar: lookup
  21. d'Ingeo S, Siniscalchi M, Quaranta A, Cousillas H, Hausberger M. Chronic State and Relationship to Humans Influence How Horses Decode Emotions in Human Voices: A Brain and Behavior Study. Animals (Basel) 2025 Nov 5;15(21).
    doi: 10.3390/ani15213217pubmed: 41227547google scholar: lookup
  22. Jardat P, Yamamoto S, Ringhofer M, Tanguy-Guillo N, Parias C, Reigner F, Calandreau L, Lansade L. Emotional contagion of fear and joy from humans to horses using a combination of facial and vocal cues. Sci Rep 2025 May 21;15(1):17689.
    doi: 10.1038/s41598-025-98794-3pubmed: 40399542google scholar: lookup
  23. Haussler KK, le Jeune SS, MacKechnie-Guire R, Latif SN, Clayton HM. The Challenge of Defining Laterality in Horses: Is It Laterality or Just Asymmetry?. Animals (Basel) 2025 Jan 21;15(3).
    doi: 10.3390/ani15030288pubmed: 39943060google scholar: lookup
  24. d'Ingeo S, Straziota V, Siniscalchi M, Depalma O, Petrassi S, Romano M, Quaranta A. Animal-Assisted Interventions: Factors Affecting Donkey Behaviours and Attitude Toward Humans. Animals (Basel) 2024 Nov 1;14(21).
    doi: 10.3390/ani14213139pubmed: 39518861google scholar: lookup
  25. Crews T, Vonk J, McGuire M. Catcalls: exotic cats discriminate the voices of familiar caregivers. PeerJ 2024;12:e16904.
    doi: 10.7717/peerj.16904pubmed: 38371372google scholar: lookup
  26. Gueguen L, Henry S, Delbos M, Lemasson A, Hausberger M. Selected Acoustic Frequencies Have a Positive Impact on Behavioural and Physiological Welfare Indicators in Thoroughbred Racehorses. Animals (Basel) 2023 Sep 20;13(18).
    doi: 10.3390/ani13182970pubmed: 37760370google scholar: lookup