Many people suffering from vestibular disorders often complain of balance problems and loss of spatial orientation. Yet, our knowledge regarding sensory (perceptual) recovery after vestibular damage remains limited and all we currently know about vestibular compensation has been based primarily on VOR deficits. Furthermore, neurophysiology experiments characterizing vestibular compensation have made no attempt to measure interneuronal correlations or correlations between neural activity and behavior (e.g., choice probabilities CP); both of which affect population decoding for sensory perception. There are three goals in the present experiments. First, we will compare neuronal thresholds in the vestibular (VN) and cerebellar (CN) nuclei, as well as parietoinsular vestibular cortex (PIVC) simultaneously as trained animals perform rotation discrimination tasks to test contemporary theories of sensory encoding and decoding. Second, we will characterize deficits and compensation in vestibular rotation perception after unilateral labyrinthectomy (UL). Results will not only be informative for vestibular rehabilitation and recovery of function, but will also provie vital tests of computational theories of sensory perception. Third, we will investigate whether noise in semicircular canal afferents contributes to perception. While macaques perform a direction discrimination task, we will search for trial-to-trial correlations between canal afferen activity and perception. Such correlations, often found in cortical neurons, are thought to reflect top-down influences. The present experiments seek to provide evidence for or against an opposite, bottom-up, hypothesis, i.e., that sensory noise propagates through to the decision. The proposed experiments represent a paradigm-shift for studying neural processing in the vestibular system. The outcomes of the proposed studies will not only be very useful for understanding perceptual deficits and recovery of spatial orientation, but will also contribute valuable and important knowledge about sensory processing and neuronal variability more generally.

Public Health Relevance

Vestibular deficits due to lesion lead to profound postural instability and loss of spatial orientation, but neurological correlates of spatial orientation disorders are still a mystery, thus posing a major hurdle in defining effective therapeutic strategies. Understanding the perceptual-related properties of the peripheral and central vestibular system for self-motion perception are vital and long-overdue. The experiments proposed here aim at filling a very notable gap in knowledge, important for understanding and treating basic postural and spatial orientation deficits.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC004260-22
Application #
9848113
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Poremba, Amy
Project Start
1999-09-01
Project End
2020-08-31
Budget Start
2019-09-01
Budget End
2020-08-31
Support Year
22
Fiscal Year
2019
Total Cost
Indirect Cost
Name
New York University
Department
Neurosciences
Type
Schools of Arts and Sciences
DUNS #
041968306
City
New York
State
NY
Country
United States
Zip Code
10012
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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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