Macaque amygdala, claustrum and pulvinar support the cross-modal association of social audio-visual stimuli based on meaning

Abstract

Social communication draws on several cognitive functions such as perception, emotion recognition and attention. In a previous study, we demonstrated that macaques associate audiovisual information when processing their species-specific communicative signals. Specifically, cortical activation is inhibited when there is a mismatch between vocalisations and social visual information whereas activation is enhanced in the lateral sulcus, superior temporal sulcus as well as a larger network composed of early visual and prefrontal areas when vocalisations and social visual information match. Here, we use a similar task and functional magnetic resonance imaging to assess the role of subcortical structures. We identify three subcortical regions involved in audio-visual processing of species-specific communicative signal: the amygdala, the claustrum and the pulvinar. Like the cortex, these subcortical structures are not activated when there is a mismatch between visual and acoustic information. In contrast, the amygdala and claustrum are activated by visual, auditory congruent and audio-visual stimulations. The pulvinar responds in a task-dependent manner, along a specific spatial sensory gradient. Anterior pulvinar responds to auditory stimuli, medial pulvinar is activated by auditory, audio-visual and visual stimuli and the dorsal lateral pulvinar only responds to visual stimuli in a pure visual task. The medial pulvinar and the amygdala are the only subcortical structures integrating audio-visual social stimuli. We propose that these three structures belong to a multisensory network that modulates the perception of visual socioemotional information and vocalizations as a function of the relevance of the stimuli in the social context. Significance StatementUnderstanding and correctly associating socioemotional information across sensory modalities, such that happy faces predict laughter and escape scenes screams, is essential when living in complex social groups. Using functional magnetic imaging in the awake macaque, we identify three subcortical structures - amygdala, claustrum and pulvinar - that only respond to auditory information that matches the ongoing visual socioemotional context, such as hearing positively valenced coo calls and seeing positively valenced grooming monkeys. We additionally describe task-dependent activations in the pulvinar, organizing along a specific spatial sensory gradient, supporting its role as a network regulator.