The programme of work is built around a framework that emphasises the role of a subcortical network comprising the hypothalamic oxytocin system, the amygdala and the superior colliculus in social attention and 'mind-reading', i.e. our ability to accurately interpret non-verbal cues produced by other individuals, which underpins a wide range of social behaviours. The methodology adopted combines behavioural approaches (cognitive laboratory tasks, WP1; naturalistic tasks in a semi-ethological setting, WP4) and brain-level approaches (neural recordings, WP2; reversible oxytocin activation and inactivation, WP3). The work in WP1 since the beginning of the project aimed to implement a novel attention coordination task in which monkey subjects learned to engage in joint attention with a realistic and interactive monkey avatar. Preliminary results show that monkeys can follow gaze cues from their avatar partner and coordinate their behaviour with it in a flexible manner.
This task will be used in WP2 to investigate the role of key subcortical structures in encoding the significance of other’s gaze shift. WP2 also aims to provide a comprehensive characterisation of neural functional specialisations with regard to social signal processing. To this end, we recorded, for the first time, the response properties of neurons in two oxytocin-rich hypothalamic subregions, the paraventricular (PVN) and supraoptic (SON) nuclei. Preliminary results highlight the sensitivity of PVN and SON neurons to different sensory stimuli (visual, acoustic, tactile), with some of them showing a preference for social over non-social stimuli. These results provide new insights into the responsiveness of the oxytocin (OT) system and provide a better understanding of how oxytocin dynamically shapes adaptive social behaviour in primates.
In WP3, we are pioneering the of use DREADDs, a technology similar to gene therapy, to enable the selective and reversible activation of oxytocin neurons in the monkey brain. In short, a viral vector is used to introduce new genetic material into OT neurons, so that these cells begin to express an excitatory receptor. This receptor can then be activated by administration of its ligand, resulting in activation of the neurons and release of oxytocin. We found that activation of OT neurons modulated the monkeys' visual attention, significantly increasing the time spent exploring socially relevant information, and in particular the eye region, in images of conspecifics. We were also able to verify that DREADD expression was restricted to OT neurons, using an immunohistochemical approach on ex-vivo brain tissue.
WP4 extends our study of social behaviour into an ethological framework allowing us to conduct brain/behaviour studies in socially interacting monkeys that move freely and express species-specific behaviour without constraint. Work in WP4 since the beginning of the project has included the development of automatic behaviour recognition from video recordings using state-of-the-art machine learning approaches, the implementation of a behavioural paradigm to test the effects of endogenous oxytocin, the collection of neural data using a wireless recording device. In the latter task, we recorded from regions of the frontal cortex while the monkeys performed kinematically similar, but different actions depending on whether they occurred in a social or non-social context (e.g. grasping during foraging or during social grooming). Most interestingly, the recorded cellular activity showed context-dependent modulation and specific responses to vocalisations.
