To navigate and act effectively through a complex three-dimensional (3D) environment, we must accurately estimate our own motion and orientation relative to nearby objects. Although multi-modal in nature, both the perception of self-motion and self-orientation, as well as the precise monitoring of changes in our head or gaze relative to objects of interest, require contributions from the vestibular system, which provides information about the angular and linear acceleration of the head in space. The long-term goal of these studies is to understand the thalamo-cortical processing of vestibular information, pertinent to the elucidation of the neural correlates for motion perception, spatial orientation and control of movement. As a first step in delineating these unexplored neural correlates of higher vestibular processing, we propose here to characterize pre-cortical neural pathways, focusing first on the neural processing in the two main thalamic projections from the vestibular nuclei (VN) and prepositus hypoglossi (PH) to the ventral posterior nuclei (VPN) and the intralaminar nuclei (ILN) of the thalamus. Experiments proposed here are motivated by a central hypothesis where these two vestibulo-thalamic pathways participate in two distinct functions: The VPN pathway represents the conduit of vestibular signals involved in selfmotion perception. The ILN pathway, on the other hand, provides cortical eye fields with the necessary extraretinal signals (including an efference copy of gaze changes) required to update retinal information for nonretinotopic saccades. To address the validity of these hypotheses, we propose a multi-faceted approach using multiple techniques, including single unit recording, antidromic identification of physiologically-characterized neurons, dual tracer injections, as well as reversible inactivation while animals perform behavioral tasks. The proposed experiments will test for the first time a direct link between vestibular neural activities and perception and will bridge the gap between traditional vestibular system analysis and modern, functionally-relevant, stochastic correlation analysis techniques relating neural activities with animal's behavioral choices.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC004260-10
Application #
7475078
Study Section
Special Emphasis Panel (ZRG1-IFCN-A (05))
Program Officer
Platt, Christopher
Project Start
1999-09-01
Project End
2009-11-30
Budget Start
2008-09-01
Budget End
2009-11-30
Support Year
10
Fiscal Year
2008
Total Cost
$313,598
Indirect Cost
Name
Washington University
Department
Neurosciences
Type
Schools of Medicine
DUNS #
068552207
City
Saint Louis
State
MO
Country
United States
Zip Code
63130
Laurens, Jean; Angelaki, Dora E (2018) The Brain Compass: A Perspective on How Self-Motion Updates the Head Direction Cell Attractor. Neuron 97:275-289
Laurens, Jean; Angelaki, Dora E (2017) A unified internal model theory to resolve the paradox of active versus passive self-motion sensation. Elife 6:
Laurens, Jean; Liu, Sheng; Yu, Xiong-Jie et al. (2017) Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex. Elife 6:
Chen, Aihua; Gu, Yong; Liu, Sheng et al. (2016) Evidence for a Causal Contribution of Macaque Vestibular, But Not Intraparietal, Cortex to Heading Perception. J Neurosci 36:3789-98
Laurens, Jean; Kim, Byounghoon; Dickman, J David et al. (2016) Gravity orientation tuning in macaque anterior thalamus. Nat Neurosci 19:1566-1568
Pitkow, Xaq; Liu, Sheng; Angelaki, Dora E et al. (2015) How Can Single Sensory Neurons Predict Behavior? Neuron 87:411-23
Yu, Xiong-jie; Dickman, J David; DeAngelis, Gregory C et al. (2015) Neuronal thresholds and choice-related activity of otolith afferent fibers during heading perception. Proc Natl Acad Sci U S A 112:6467-72
Yu, Xiong-Jie; Thomassen, Jakob S; Dickman, J David et al. (2014) Long-term deficits in motion detection thresholds and spike count variability after unilateral vestibular lesion. J Neurophysiol 112:870-89
Liu, Sheng; Gu, Yong; DeAngelis, Gregory C et al. (2013) Choice-related activity and correlated noise in subcortical vestibular neurons. Nat Neurosci 16:89-97
Liu, Sheng; Dickman, J David; Newlands, Shawn D et al. (2013) Reduced choice-related activity and correlated noise accompany perceptual deficits following unilateral vestibular lesion. Proc Natl Acad Sci U S A 110:17999-8004

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