Chronic State and Relationship to Humans Influence How Horses Decode Emotions in Human Voices: A Brain and Behavior Study

TL;DR

Horses from different living conditions react differently to human emotions in voices, with better welfare and stable relationships leading to calmer responses.

Contribution

The study reveals that horses' emotional decoding of human voices is influenced by their welfare state and human relationships, not just universal cues.

Findings

Horses in poor welfare and unstable relationships showed stronger reactions to negative emotional voices.

Horses with better welfare and stable relationships reacted calmly and showed interest in positive voices.

Brain activity differences were observed, with distinct patterns for each population based on emotional cues.

Abstract

Understanding how animals perceive human emotions is important for improving their welfare and our interactions with them. In this study, we examined how two groups of horses reacted to human voices expressing different emotions, such as happiness, anger, fear, and sadness. The horses came from very different environments: one group lived in more natural and stable social conditions, with interactions with only a few familiar humans, while the other group lived in more restricted housing and had frequent contact with many different riders. We found that horses in poorer welfare states (assessed by animal-based measures) and with less stable relationships with humans showed stronger behavioral and physiological reactions to negative emotional voices. In contrast, horses in better welfare states reacted more calmly and showed more interest in positive voices. Brain activity also reflected these differences, suggesting that both emotional state and life experience play a role in how animals perceive human emotions. These findings show that animals do not respond to emotional signals in a universal way; their individual history matters. This knowledge can help improve how we care for and interact with animals, particularly in training, handling, and welfare assessment.

Current research on acoustic encoding of emotional content suggests that there are universal cues, allowing for decoding within and across taxa. This is particularly important for human–animal relationships, wherein domestic animals are supposed to be particularly efficient in decoding human emotions. Here we investigated whether the decoding of the emotional content in human voices shared universal acoustic properties, or whether it could be influenced by experience. Emotional human voices were presented to two populations of horses, in which behavioral, cardiac, and brain responses were measured. The two populations differed in their living and working conditions: one population lived in naturalistic conditions (stable social groups in pastures) and were ridden occasionally for outdoor trail riding with one to a few different riders, while the other was kept in more restricted conditions (individual stalls) and participated in riding lessons involving many different riders. Assessment of the horses’ welfare state (animal-based measures) and their relationships with humans, performed independently of the playback experiments, revealed that the populations differed in both aspects. Whereas both populations appeared to react to the angry human voice, the population with the best welfare state and relationship with humans showed little differentiation between the different emotional voices and exhibited low behavioral reactions. On the contrary, the other population showed high behavioral and cardiac reactions to all negative voices. Brain responses also differed, with the first population showing higher responses (increased gamma, i.e., excitation) for the happy voice and the second for fear and anger (increased theta, i.e., alarm). Thus, animals’ affective state and past experiences appear very influential for their perception of (cross-taxa) acoustic emotional cues.

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