Many animals can detect and use the Earth's magnetic field for orientation and navigation functions. We have recently discovered cells in the vestibular brainstem of pigeons that encode the direction and intensity of the magnetic field (MR cells); as well as being multisensory carrying vestibular linear motion signals. We have also characterized a magnetic sense neural pathway that includes regions in the brain known to be involved with spatial orientation and navigation tasks, including the vestibular nuclei, dorsal thalamus, hippocampus, and visual association cortex. The primary goal of the proposed project is to determine how multisensory convergence of vestibular and magnetic sense signals creates neural constructs that encode geopositional and heading direction information. First, we found that MR cells are spatially cosine tuned to magnetic field direction, thus these neurons encode a 3D magnetic field vector.
In Aim 1, we will examine whether magnetic directional tuning is referenced to the world-fixed constant of gravity. We hypothesize that multisensory integration of vestibular and magnetic cues allows MR cell directional responses to be spatially stable and not change with head position.
In Aim 2, we will determine if MR cell translational responses are fixed relative to the magnetic field direction, independent of head position. We hypothesize that MR cells provide directional heading information in magnetic field coordinates. We recently also discovered that the distinct state of gliding flight increases the sensitivity to motion in vestibuar neurons.
In Aim 3, we will determine if flight increases the sensitivity of MR cells and provides for more complete reference frame transformations as outlined in Aims 1 and 2. Together, these experiments will uncover basic multisensory integration mechanisms for building neural representations of position and heading direction. These are vital functions for all animal behavior and are often compromised by vestibular trauma or disease in people. Understanding how a new magnetic sense uses vestibular motion cues through convergence to create complex information constructs will provide key insights into important brain functions and bring us closer to obtaining new treatment options disorientation maladies.

Public Health Relevance

We have discovered brainstem neurons that combine cues from vestibular motion and magnetic sense signals to contribute to orientation in birds whose lives depend upon long distance navigation. This beautiful ability to home and migrate is demonstrated by most vertebrates and utilizes little understood abilities to detect and process information regarding the Earth's geomagnetic field. Understanding how the brain uses multisensory cues to perform computational constructs that underlie orientation function will provide specific insights into the disorientation problems people suffer with vestibular function loss.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
4R01DC012813-04
Application #
8960930
Study Section
Auditory System Study Section (AUD)
Program Officer
Platt, Christopher
Project Start
2012-12-01
Project End
2017-11-30
Budget Start
2015-12-01
Budget End
2016-11-30
Support Year
4
Fiscal Year
2016
Total Cost
Indirect Cost
Name
Baylor College of Medicine
Department
Neurosciences
Type
Schools of Medicine
DUNS #
051113330
City
Houston
State
TX
Country
United States
Zip Code
77030
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Zakir, M; Wu, L-Q; Dickman, J D (2012) Morphology and innervation of the vestibular lagena in pigeons. Neuroscience 209:97-107
Wu, Le-Qing; Dickman, J David (2011) Magnetoreception in an avian brain in part mediated by inner ear lagena. Curr Biol 21:418-23
McArthur, K L; Zakir, M; Haque, A et al. (2011) Spatial and temporal characteristics of vestibular convergence. Neuroscience 192:361-71
McArthur, Kimberly L; Dickman, J David (2011) State-dependent sensorimotor processing: gaze and posture stability during simulated flight in birds. J Neurophysiol 105:1689-700
McArthur, Kimberly L; Dickman, J David (2011) Behavioral state modulates the activity of brainstem sensorimotor neurons. J Neurosci 31:16700-8