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

Marcello Siniscalchi,Angelo Quaranta,Martine Hausberger,Hugo Cousillas,Mathilde Stomp,Caroline Coste,Serenella D’Ingeo,Charlotte Bagnard

doi:10.1038/s41598-019-47960-5

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.

Highlights

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
The results show that horses reacted to voices associated with past positive experiences with increased attention/ arousal and indicators of a positive emotional state, and to those associated with past negative experiences with negative affective states
To date the studies on animals have only reported broad differences between right-left hemisphere activation in response to emotional acoustic stimuli, a recent study, examining the dog brain areas involved in processing acoustic stimuli, identified a specific region in dogs’ auditory cortex, namely the right caudal ectosylvian gyri, which is sensitive to the emotional valence of vocalization and is strongly activated in response to positive vocalizations of both humans and conspecifics[26]

Summary

Introduction

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. Www.nature.com/scientificreports right hemisphere dominant activity has been shown in response to intraspecific or heterospecific vocalizations related to a negative valence in cats[8], monkeys[19,20], dogs[21] and horses[22], supporting the general hypothesis of the right hemisphere main involvement in processing intense emotions and arousing stimuli[23,24]. To date the studies on animals have only reported broad differences between right-left hemisphere activation in response to emotional acoustic stimuli, a recent study, examining the dog brain areas involved in processing acoustic stimuli, identified a specific region in dogs’ auditory cortex, namely the right caudal ectosylvian gyri (cESG), which is sensitive to the emotional valence of vocalization and is strongly activated in response to positive vocalizations of both humans and conspecifics[26]. These findings suggest that dogs and horses are sensitive to the emotional content of human vocalizations

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Results

Conclusion