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 audio-visual 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.

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

“…This possibly sheds new light on the functional organization of this subcortical nucleus. Further investigation in humans and non‐human primates are needed to further consolidate these observations, including by manipulating context in different ways, as well as to further study the precise functional connectivity of the pulvinar with the cortex (Froesel et al, 2023). In addition to this cross‐modal associations of communicative signals, the medial part of the pulvinar and the dorsolateral amygdala show a greater activation to the bimodal audio‐visual stimulation relative to each of the visual and auditory unimodal stimulations.…”

Multiple focal pulvinar projection fields in the macaque cortex

“…These projections from multiple pulvinar nuclei in specific brain regions has been a core argument in support of the role of the pulvinar as a modulator (Benarroch, 2015; Saalmann & Kastner, 2011). The pulvinar can thus be a part of several networks and can be recruited differentially as a function of sensory modality or the ongoing cognitive demand (Froesel et al, 2022), thus supporting cognitive flexibility. As a result, another important aspect to keep in mind is that the winner-take-all maps we report here from monkeys at rest could be different during active tasks involving either sensory stimulation or the production of complex behaviors.…”