We investigate an important function of the vestibular system, and its multisensory properties, in spatial navigation, specifically head direction (HD) cells. HD cells encode directional heading like a compass and these properties are generated through a ring attractor network that is defined by orienting landmarks and updated using self-motion velocity cues. The goal of this renewal application is to establish the principles and circuits linking vestibular signals to HD cells in the anterior thalamus, through three aims. In the first two aims we will thoroughly test theory-driven hypotheses about the self-motion signal that updates the ring attractor. We will disentangle two contributions to HD tuning strength: self-motion velocity input, and brain state, which we hypothesize exerts a tonic modulatory role on the intrinsic properties of the attractor itself. We will show that passive rotations are as effective in updating the HD attractor as active foraging, and will test model-driven hypotheses about their multisensory properties.
In Aim 3 we will genetically and optogenetically manipulate large or discrete regions of the cerebellum while monitoring the activity of HD cells in anterodorsal and laterodorsal thalamus. The hypothesized role of multisensory cerebellar signals is 2-fold: to help maintain internal models about 1) rotation velocity, and 2) gravity. The former updates the firing and the latter defines the 3D tuning of HD cells. Collectively, these experiments will provide a long-overdue, thorough and quantitative understanding of the multisensory properties of one of the most important components of the spatial navigation circuit. Our strength is an interdisciplinary approach based on a quantitative understanding of both multisensory and computational neuroscience, which promises novel insights into the organization of the spatial properties of HD cells and their links with the vestibular system.
When our sense of spatial orientation is compromised by limbic system lesions or Alzheimer?s disease, devastating effects upon our ability to orient in familiar environments, navigate from place to place, or even find our way home can occur. The current project seeks to test theory-driven hypotheses about the multisensory signals updating head direction cells in the rodent anterior thalamus and cortex, areas critically linked to spatial orientation and spatial memory disorders.
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