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

Social communication draws on several cognitive functions such as perception, emotion recognition and attention. The association of audio-visual information is essential to the processing of species-specific communication signals. In this study, we use functional magnetic resonance imaging in order to identify the subcortical areas involved in the cross-modal association of visual and auditory information based on their common social meaning. We identified three subcortical regions involved in audio-visual processing of species-specific communicative signals: the dorsolateral amygdala, the claustrum and the pulvinar. These regions responded to visual, auditory congruent and audio-visual stimulations. However, none of them was significantly activated when the auditory stimuli were semantically incongruent with the visual context, thus showing an influence of visual context on auditory processing. For example, positive vocalization (coos) activated the three subcortical regions when presented in the context of positive facial expression (lipsmacks) but not when presented in the context of negative facial expression (aggressive faces). In addition, the medial pulvinar and the amygdala presented multisensory integration such that audiovisual stimuli resulted in activations that were significantly higher than those observed for the highest unimodal response. Last, the pulvinar responded in a task-dependent manner, along a specific spatial sensory gradient. We propose that the dorsolateral amygdala, the claustrum and the pulvinar 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 STATEMENT: Understanding and correctly associating socioemotional information across sensory modalities, such that happy faces predict laughter and escape scenes predict screams, is essential when living in complex social groups. With the use of functional magnetic imaging in the awake macaque, we identify three subcortical structures-dorsolateral 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 mutual 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.

Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain.

Social interactions rely on the interpretation of semantic and emotional information, often from multiple sensory modalities. Nonhuman primates send and receive auditory and visual communicative signals. However, the neural mechanisms underlying the association of visual and auditory information based on their common social meaning are unknown. Using heart rate estimates and functional neuroimaging, we show that in the lateral and superior temporal sulcus of the macaque monkey, neural responses are enhanced in response to species-specific vocalisations paired with a matching visual context, or when vocalisations follow, in time, visual information, but inhibited when vocalisation are incongruent with the visual context. For example, responses to affiliative vocalisations are enhanced when paired with affiliative contexts but inhibited when paired with aggressive or escape contexts. Overall, we propose that the identified neural network represents social meaning irrespective of sensory modality.

Automated video-based heart rate tracking for the anesthetized and behaving monkey.

Heart rate (HR) is extremely valuable in the study of complex behaviours and their physiological correlates in non-human primates. However, collecting this information is often challenging, involving either invasive implants or tedious behavioural training. In the present study, we implement a Eulerian video magnification (EVM) heart tracking method in the macaque monkey combined with wavelet transform. This is based on a measure of image to image fluctuations in skin reflectance due to changes in blood influx. We show a strong temporal coherence and amplitude match between EVM-based heart tracking and ground truth ECG, from both color (RGB) and infrared (IR) videos, in anesthetized macaques, to a level comparable to what can be achieved in humans. We further show that this method allows to identify consistent HR changes following the presentation of conspecific emotional voices or faces. EVM is used to extract HR in humans but has never been applied to non-human primates. Video photoplethysmography allows to extract awake macaques HR from RGB videos. In contrast, our method allows to extract awake macaques HR from both RGB and IR videos and is particularly resilient to the head motion that can be observed in awake behaving monkeys. Overall, we believe that this method can be generalized as a tool to track HR of the awake behaving monkey, for ethological, behavioural, neuroscience or welfare purposes.