Sheffield, A. G. | bioRxiv Science

bioRxiv2024

Automated 3D analysis of social head-gaze behaviors in freely moving marmosets

Social communication relies on the ability to perceive and interpret the direction of others attention, and is commonly conveyed through head orientation and gaze direction in humans and nonhuman primates. However, traditional social gaze experiments in nonhuman primates require restraining head movements, significantly limiting their natural behavioral repertoire. Here, we developed a novel framework for accurately tracking facial features and three-dimensional head gaze directions of multiple freely moving common marmosets (Callithrix jacchus). By combining deep learning-based computer vision tools with triangulation algorithms, we were able to track the facial features of marmoset dyads within an arena. This method effectively generates dynamic 3D geometrical facial frames while overcoming common challenges like occlusion. To detect the head gaze direction, we constructed a virtual cone, oriented perpendicular to the facial frame. Using this pipeline, we quantified different types of interactive social gaze events, including partner-directed gaze and joint gaze to a shared spatial location. We observed clear effects of sex and familiarity on both interpersonal distance and gaze dynamics in marmoset dyads. Unfamiliar pairs exhibited more stereotyped patterns of arena occupancy, more sustained levels of social gaze across social distance, and increased social gaze monitoring. On the other hand, familiar pairs exhibited higher levels of joint gazes. Moreover, males displayed significantly elevated levels of gazes toward females faces and the surrounding regions, irrespective of familiarity. Our study reveals the importance of two key social factors in driving the gaze behaviors of a prosocial primate species and lays the groundwork for a rigorous quantification of primate behaviors in naturalistic settings.

animal behavior and cognition↗

bioRxiv2023

State-dependent modulation of dependencies in a laminar cortical circuit

Spatial attention is a quintessential example of adaptive information processing in the brain and is critical for recognizing behaviorally relevant objects in a cluttered environment. Object recognition is mediated by neural encoding along the ventral visual hierarchy. How the deployment of spatial attention aids these hierarchical computations is unclear. Prior studies point to two distinct mechanisms: an improvement in the efficacy of information directed from one encoding stage to another1-5, and/or a suppression of shared information within encoding stages6,7. To test these proposals, it is crucial to estimate the attentional modulation of unique information flow across and shared information within the encoding stages of the visual hierarchy. We investigated this in the multi-stage laminar network of visual area V4, an area strongly modulated by attention8-10. Using network-based dependency estimation from multivariate data, we quantified the modulation of inter-layer information flow during a change detection task and found that deployment of attention indeed strengthened unique dependencies between the input and superficial layers. Using the partial information decomposition framework11,12, we estimated the modulation of shared dependencies and found that they are reduced specifically in the putative excitatory subpopulations within a layer. Surprisingly, we found a strengthening of unique dependencies within the laminar populations, a finding not previously predicted. Crucially, these modulation patterns were also observed during successful behavioral outcomes (hits) that are thought to be mediated by endogenous brain state fluctuations13-15, and not by experimentally imposed attentive states. Finally, phases of endogenous fluctuations that were optimal for hits were associated with reduced neural excitability. A reduction in neural excitability, potentially mediated by diminished shared inputs, suggests a novel mechanism for enhancing unique information transmission during optimal states. By decomposing the modulation of multivariate information, and combined with prior theoretical work16, our results suggest common computations of optimal sensory states that are attained by either task demands or endogenous fluctuations.

neuroscience↗