Emotional valence of conspecific vocalizations modulates auditory and limbic brain activity in juvenile pigs

Abstract

Pig vocalizations convey information about the emotional states of individuals, varying with arousal and valence. Studies show that different call types reflect distinct emotional contexts and social interactions for the receivers. However, little is known about the brain mechanisms behind the perception of conspecifics vocalizations. This study used BOLD fMRI to explore how pigs brains respond to emotionally varied vocalizations, with the aim to identify activity in regions linked to emotion, reward, and social processing. Eight healthy 2-month-old pigs underwent auditory brainstem response (ABR) testing and BOLD fMRI to assess brain responses to pig vocalizations with different hedonic valence. Sounds were delivered via MRI-compatible earphones, and imaging was performed on a 1.5T scanner. Data were analyzed using voxel-based and ROI-based statistics in SPM12 with small volume correction (SVC). Due to hearing anomalies or MRI artefacts, only 5 pigs were included in the final analysis. Functional MRI revealed that vocalizations activated regions of the auditory pathway and the left amygdala (pFWE at peak < 0.05 after SVC for all), with specific differences between positive and negative sounds. Clusters of activated voxels covering part of hippocampal areas, caudate nuclei and putamen were found with both positive and aversive vocal sounds. Limbic regions, including the amygdala and insula (p<0.05), as well as the right hippocampus after SVC (pFWE = 0.015) were uniquely engaged during the perception of negative conspecific vocalizations, indicating distinct processing based on emotional valence. This study shows for the first time that piglets brain can process and differentiate emotional vocalizations from other pigs, even under general anesthesia. Positive and negative vocal sound playbacks activated distinct brain regions related to hearing, emotion and reward. These findings highlight pigs cognitive and emotional processing of vocal cues. This study is part of a wider research program aimed at developing the fMRI protocol with acoustic stimulation in juvenile pigs.