Neural Substrates for Visual Decision Making in the Visual Cortex

National Eye Institute

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Abstract

During the past funding period we made progress in five projects: 1) Organisms process sensory information in the context of their own moving bodies, an idea referred to as embodiment. This idea is important for developmental neuroscience, and increasingly plays a role in robotics and systems neuroscience. The mechanisms that support such embodiment are unknown, but a manifestation could be the observation in mice of brain-wide neuromodulation, including in the primary visual cortex, driven by task-irrelevant spontaneous body movements. In this project we tested this hypothesis in macaque monkeys, a primate model for human vision, by simultaneously recording visual cortex activity and facial and body movements. Activity in the visual cortex (V1, V2, V3/V3A) was associated with the animals own movements, but this modulation was largely explained by the impact of the movements on the retinal image. These results suggest that embodiment in primate vision may be realized by input provided by the eyes themselves. In follow up work on these results we are examine the modulatory influence of task-engagement, physiological state and arousal on neural activity in the early visual cortex. 2) Exploring the flexibility or processing across tasks in mid-level visual processing and higher sensorimotor areas: Anatomical feedback connections are a ubiquitous property of the cerebral cortex but its role for computation and behavior is not understood. One of the most substantial differences between biological and state-of-the art artificial vision circuits concerns feedback: artificial systems typically do not incorporate feedback, whereas feedback is evident between every stage in the visual-processing hierarchy. This discrepancy underscores the large gap in our knowledge about the role of feedback in visual processing. A prediction common to theoretical accounts of feedback is that it targets the relevant neuronal subpopulations. For simple settings, this is supported by decades of empirical findings: If a localized region of space is relevant to a behavioral task, processing at that region can be selectively enhanced by feedback (spatial attention). If a given visual feature is relevant, processing of that feature can be selectively modulated throughout the visual field (feature selective attention). But the real world is more complex than such simple settings. Oftentimes behaviors depend on some combination of mechanisms, and whatever mechanisms enable behavior need to be flexibly and dynamically deployed, and in light of the enormous number of ethologically possible tasks and contexts, such selectivity could become anatomically costly. In this project we trained animals to perform a visual discrimination task that combines aspects of both feature and visual space, and we leverage a powerful behavioral analysis tool that enables us to be certain about what aspect of the task is used by the animal in making its decision. While the animals performed the task, we used multi-contact neurophysiological array recordings targeted at mid-level visual areas (V2, V3, V3a). We found that while the animals behavior was highly spatially selective, the task-relevant feedback was not. It suggests a common mechanism across tasks, independent of the spatial selectivity those tasks demand. Such common mechanism may reflect biological contraints to limit the anatomical cost of the feedback, while facilitating generalization across tasks (Quinn et al. 2021). We are now expanding on these findings to examine signal processing across the visual and visuomotor hierarchy while the animals perform this task that requires flexible use of visual information and relies on flexible ways to report the decisions. 3) Selectivity for binocular disparity in the primate superior colliculus (SC). Many of our task use binocular disparity based tasks to address questions about visually guided decisions in rhesus macaques. The superior colliculus is an important structure involved in such visually driven behavior, but it is unknown to date, whether it itself shows selectivity for binocular disparity. In a collaborative project with Rich Krauslis' group we discovered that a majority of neurons in the SC show selectivity for binocular disparity in ways that appear more closely linked to perception than the primary visual cortex, V1. 4) With the ability to collect increasingly high-dimensional behavioral and neural data, we need ways to characterize and quantify relevant behavioral features in an unbiased way, in order to relate these to neural signals. To address this challenge summary statistics or hand-picked features are often used. But by doing so it is possible that information about the underlying structure of the data is missed. We used a model-based approach using GLMs (generalized linear models) on a comprehensive dataset of eye measurements and neurophysiological data while animals performed a complex visual task requiring switches in spatial attention. This unbiased approach separate modulatory influences of spatial attention and characteristic eye-movements (microsaccades) on neural activity. We are currently preparing these results for publication. 5) In collaboration with Wei Li's lab at the NEI we examine the role of hibernation in ground squirrels, as one pronounced form of change in behavioral/physiological state, on plasticity in the primary visual cortex. Our results showed that substantial, hibernation related plasticity extended to the primary visual cortex, and differs across cell types. We are currently preparing these results for publication.