Abstract
Recently, research on domestic mammals’ sociocognitive skills toward humans has been prolific, allowing us to better understand the human–animal relationship. For example, horses have been shown to distinguish human beings on the basis of photographs and voices and to have cross-modal mental representations of individual humans and human emotions. This leads to questions such as the extent to which horses can differentiate human attributes such as age. Here, we tested whether horses discriminate human adults from children. In a cross-modal paradigm, we presented 31 female horses with two simultaneous muted videos of a child and an adult saying the same neutral sentence, accompanied by the sound of an adult’s or child’s voice speaking the sentence. The horses looked significantly longer at the videos that were incongruent with the heard voice than at the congruent videos. We conclude that horses can match adults’ and children’s faces and voices cross-modally. Moreover, their heart rates increased during children’s vocalizations but not during adults’. This suggests that in addition to having mental representations of adults and children, horses have a stronger emotional response to children’s voices than adults’ voices.
Similar content being viewed by others
Data availability
The datasets generated and analyzed during the current study are available in the INRAE data repository from the following link: https://doi.org/10.15454/SKHGKZ
References
Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner’s face upon hearing the owner’s voice. Anim Cogn 10:17–21. https://doi.org/10.1007/s10071-006-0025-8
Albuquerque N, Guo K, Wilkinson A et al (2016) Dogs recognize dog and human emotions. Biol Lett 12:20150883. https://doi.org/10.1098/rsbl.2015.0883
Archer J (1997) Why do people love their pets? Evol Hum Behav 18:237–259. https://doi.org/10.1016/S0162-3095(99)80001-4
Archer J, Monton S (2011) Preferences for infant facial features in pet dogs and cats. Ethology 117:217–226. https://doi.org/10.1111/j.1439-0310.2010.01863.x
Brensing K, Linke K (2003) Behavior of dolphins towards adults and children during swim-with-dolphin programs and towards children with disabilities during therapy sessions. Anthrozoos 16:315–331. https://doi.org/10.2752/089279303786992035
Briefer EF, Maigrot A-L, Mandel R et al (2015a) Segregation of information about emotional arousal and valence in horse whinnies. Sci Rep 5:9989. https://doi.org/10.1038/srep09989
Briefer EF, Tettamanti F, McElligott AG (2015b) Emotions in goats: mapping physiological, behavioural and vocal profiles. Anim Behav 99:131–143. https://doi.org/10.1016/j.anbehav.2014.11.002
Dilley LC, Wieland EA, Gamache JL et al (2013) Age-related changes to spectral voice characteristics affect judgments of prosodic, segmental, and talker attributes for child and adult speech. J Speech, Lang Hear Res 56:159–177. https://doi.org/10.1044/1092-4388(2012/11-0199)
Farkas LG, Hreczko TA, Kolar JC, Munro IR (1985) Vertical and horizontal proportions of the face in young adult North American Caucasians. Plast Reconstr Surg 75:328–337. https://doi.org/10.1097/00006534-198503000-00005
Forkman B, Boissy A, Meunier-Salaün MC et al (2007) A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiol Behav 92:340–374. https://doi.org/10.1016/j.physbeh.2007.03.016
Gácsi M, Miklód Á, Varga O et al (2004) Are readers of our face readers of our minds? Dogs (Canis familiaris) show situation-dependent recognition of human’s attention. Anim Cogn 24:144–153. https://doi.org/10.1007/s10071-003-0205-8
Glaze LE, Bless DM, Milenkovic P, Susser RD (1988) Acoustic characteristics of children’s voice. J Voice 2:312–319. https://doi.org/10.1016/S0892-1997(88)80023-7
Jardat P, Lansade L (2021) Cognition and the human–animal relationship: a review of the sociocognitive skills of domestic mammals toward humans. Anim Cogn. https://doi.org/10.1007/s10071-021-01557-6
Jardat P, Calandreau L, Ferreira V et al (2022) Pet-directed speech improves horses’ attention toward humans. Sci Rep 12:4297. https://doi.org/10.1038/s41598-022-08109-z
Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163. https://doi.org/10.1016/j.jcm.2016.02.012
Lampe JF, Andre J (2012) Cross-modal recognition of human individuals in domestic horses (Equus caballus). Anim Cogn 15:623–630. https://doi.org/10.1007/s10071-012-0490-1
Lansade L, Bouissou MF, Erhard HW (2008) Fearfulness in horses: a temperament trait stable across time and situations. Appl Anim Behav Sci 115:182–200. https://doi.org/10.1016/j.applanim.2008.06.011
Lansade L, Colson V, Parias C et al (2020a) Human face recognition in horses: data in favor of a holistic process. Front Psychol 11:2311. https://doi.org/10.3389/fpsyg.2020.575808
Lansade L, Colson V, Parias C et al (2020b) Female horses spontaneously identify a photograph of their keeper, last seen six months previously. Sci Rep 10:6302. https://doi.org/10.1038/s41598-020-62940-w
Lansade L, Trösch M, Parias C et al (2021) Horses are sensitive to baby talk: pet-directed speech facilitates communication with humans in a pointing task and during grooming. Anim Cogn 5:999–1006. https://doi.org/10.1007/s10071-021-01487-3
Lee S, Potamianos A, Narayanan S (1999) Acoustics of children’s speech: developmental changes of temporal and spectral parameters. J Acoust Soc Am 105:1455–1468. https://doi.org/10.1121/1.426686
Little AC (2012) Manipulation of infant-like traits affects perceived cuteness of infant, adult and cat faces. Ethology 118:775–782. https://doi.org/10.1111/J.1439-0310.2012.02068.X
Moyse E (2014) Age estimation from faces and voices: a review. Psychologica Belgica. Ubiquity Press Ltd, pp 255–265
Munsters CCBM, Visser KEK, van den Broek J, Sloet van Oldruitenborgh-Oosterbaan MM (2012) The influence of challenging objects and horse-rider matching on heart rate, heart rate variability and behavioural score in riding horses. Vet J 192:75–80. https://doi.org/10.1016/j.tvjl.2011.04.011
Nakamura K, Takimoto-Inose A, Hasegawa T (2018) Cross-modal perception of human emotion in domestic horses (Equus caballus). Sci Rep 8:8660. https://doi.org/10.1038/s41598-018-26892-6
Pattison KF, Miller HC, Rayburn-Reeves R, Zentall T (2010) The case of the disappearing bone: dogs’ understanding of the physical properties of objects. Behav Processes 85:278–282. https://doi.org/10.1016/J.BEPROC.2010.06.016
Proops L, Mccomb K (2012) Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans. Proc R Soc B Biol Sci 279:3131–3138. https://doi.org/10.1098/rspb.2012.0626
Proops L, Grounds K, Smith AV, McComb K (2018) Animals remember previous facial expressions that specific humans have exhibited. Curr Biol 28:1428-1432.e4. https://doi.org/10.1016/j.cub.2018.03.035
Quaranta A, D’ingeo S, Amoruso R, Siniscalchi M (2020) Emotion recognition in cats. Animals 10:1107. https://doi.org/10.3390/ani10071107
R Core Team (2013) R: a language and environment forstatistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ringhofer M, Yamamoto S (2017) Domestic horses send signals to humans when they face with an unsolvable task. Anim Cogn 20:397–405. https://doi.org/10.1007/s10071-016-1056-4
Ringhofer M, Trösch M, Lansade L, Yamamoto S (2021) Horses with sustained attention follow the pointing of a human who knows where food is hidden. Sci Rep 111(11):1–9. https://doi.org/10.1038/s41598-021-95727-8
Russell JA, Barrett LF (1999) Core affect, prototypical emotional episodes, and other things called emotion: dissecting the elephant. J Pers Soc Psychol 76:805–819. https://doi.org/10.1037/0022-3514.76.5.805
Siniscalchi M, D’Ingeo S, Quaranta A (2018) Orienting asymmetries and physiological reactivity in dogs’ response to human emotional faces. Learn Behav 46:574–585. https://doi.org/10.3758/s13420-018-0325-2
Smith AV, Proops L, Grounds K et al (2018) Domestic horses (Equus caballus) discriminate between negative and positive human nonverbal vocalisations. Sci Rep 8:13052. https://doi.org/10.1038/s41598-018-30777-z
Somppi S, Törnqvist H, Hänninen L et al (2012) Dogs do look at images: eye tracking in canine cognition research. Anim Cogn 15:163–174. https://doi.org/10.1007/s10071-011-0442-1
Stathopoulos ET, Huber JE, Sussman JE (2011) Changes in acoustic characteristics of the voice across the life span: measures from individuals 4–93 years of age. J Speech, Lang Hear Res 54:1011–1021. https://doi.org/10.1044/1092-4388(2010/10-0036)
Sussman JE, Sapienza C (1994) Articulatory, developmental, and gender effects on measures of fundamental frequency and jitter. J Voice 8:145–156. https://doi.org/10.1016/S0892-1997(05)80306-6
Takagi S, Arahori M, Chijiiwa H et al (2019) Cats match voice and face: cross-modal representation of humans in cats (Felis catus). Anim Cogn 22:901–906. https://doi.org/10.1007/s10071-019-01265-2
Trösch M, Cuzol F, Parias C et al (2019a) Horses categorize human emotions cross-modally based on facial expression and non-verbal vocalizations. Animals 9:862. https://doi.org/10.3390/ani9110862
Trösch M, Ringhofer M, Yamamoto S et al (2019b) Horses prefer to solicit a person who previously observed a food-hiding process to access this food: a possible indication of attentional state attribution. Behav Processes 166:103906. https://doi.org/10.1016/j.beproc.2019.103906
Trösch M, Bertin E, Calandreau L et al (2020a) Unwilling or willing but unable: can horses interpret human actions as goal directed? Anim Cogn 23:1035–1040. https://doi.org/10.1007/s10071-020-01396-x
Trösch M, Pellon S, Cuzol F et al (2020b) Horses feel emotions when they watch positive and negative horse–human interactions in a video and transpose what they saw to real life. Anim Cogn 23:643–653. https://doi.org/10.1007/s10071-020-01369-0
von Borell E, Langbein J, Després G et al (2007) Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals—a review. Physiol Behav 92:293–316. https://doi.org/10.1016/j.physbeh.2007.01.007
Wanser SH, Simpson AC, MacDonald M, Udell MAR (2020) Considering family dog attachment bonds: do dog-parent attachments predict dog-child attachment outcomes in animal-assisted interventions? Front Psychol 11:2293. https://doi.org/10.3389/FPSYG.2020.566910/BIBTEX
Wanser SH, MacDonald M, Udell MAR (2021) Dog-human behavioral synchronization: family dogs synchronize their behavior with child family members. Anim Cogn 24:747–752. https://doi.org/10.1007/s10071-020-01454-4
Acknowledgements
We thank Adèle, Amande, Coline, and the other volunteers who were filmed to make up the stimuli of this experiment; Estel Blasi for drawing Fig. 1; and Springer Nature Authors Services for English language and text flow editing.
Funding
This study was funded by Institut Français du Cheval et de l’Equitation (IFCE), Grant Number 32 000809-Cognition Equine.
Author information
Authors and Affiliations
Contributions
All authors devised the protocol. PJ, CG, CP, FR, and LL implemented the protocol. PJ, CG, and LL coded the videos and analyzed the data from heart rate monitoring and behavior coding. PJ, MR, SY, CG, RD, LC, and LL revised the analysis and report.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Informed consent
All the people participating in the study provided informed consent.
Ethical statement
Animal care and experimental treatments complied with the French and European guidelines for housing and care of animals used for scientific purposes (European Union Directive 2010/63/EU) and were performed under the authorization and supervision of official veterinary services (Agreement Number F371752 delivered to the UEPAO animal facility by the veterinary service of the Département d’Indre et Loire, France). This experiment was approved by the Val de Loire Ethical Committee (CEEA VdL, Nouzilly, France, Authorization Number CE19-2022-1503-1). This study was reported in accordance with ARRIVE guidelines.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Jardat, P., Ringhofer, M., Yamamoto, S. et al. Horses form cross-modal representations of adults and children. Anim Cogn 26, 369–377 (2023). https://doi.org/10.1007/s10071-022-01667-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-022-01667-9