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Ear Manipulations Reveal Importance of Gravity Input for Orientation Development
Karen Elliott Thompson
University of Iowa
On Earth
• Gravity provides linear but not angular acceleration
• In Space, astronauts experience microgravity
GRAVITY
Image from http://upload.wikimedia.org/wikipedia/commons/9/98/Aldrin_Apollo_11_original.jpg
Image from http://t.wallpaperweb.org/wallpaper/space/1280x1024/shuttle_99_2_1280.jpg
Microgravity
• ALL linear acceleration is associated with angular acceleration due to centrifugal forces acting on the inner ear
• Perceived as self-movement
Return to Gravity on Earth
• Gravity again provides linear but not angular acceleration
• Brain adds the perception of angular acceleration
• Body attempts to counter with motor and eye movements
• Results in difficulty walking, standing, and stabilizing gaze
GRAVITY
Goal
To understand how gravity shapes the nervous system to guide behavior
• Want to look at areas where synaptic plasticity in gravity perception occur
Gravity and Movement Perception • Linear Acceleration
– Utricle
– Saccule
• Angular Acceleration – Semicircular canals
Image from Kopecky et al., 2012
U
S
ac pc
hc
http://www.bthchiroonline.com/wordpress/wp-content/uploads/2012/11/inner_ear.jpg
Neuronal Network
• The plasticity between gravity input and motor output
occurs in the vestibular nuclei – Eron et al.(2008) Adaptationof orientation vectors of otolith-related central vestibular neurons to
gravity. Journal of Neurophysiology 75: 1928-1932
Brain
Spinal Cord
Experiment:
• Manipulate the gravity sensor: the ear – Remove one ear
– Add one ear
• Determine how asymmetrical and mismatched gravity detection shapes behavior and nervous system – Swimming
– Sensory projections
– Target neuron
Image from: http://petra-aqua.com/gfx/foto/1954.jpg
http://www.shechterlab.org/wp-content/uploads/2009/08/frog-eggs.jpg
Transplantation Method
• Donor ear from a Xenopus embryo (stage 25-27) is transplanted to host, rostral to native ear
– Ear in native orientation
– Ear rotated by 90 degrees
1-eared animal 3-eared animal
Transplantation Method
• Donor ear from a Xenopus embryo (stage 25-27) is transplanted to host, rostral to native ear
– Ear in native orientation
– Ear rotated by 90 degrees
• Embryos allowed to grow until early tadpole (stage 46)
• Swimming monitored
Rationale
• Native orientation – Sensory epithelia
aligned – Respond the same to
a given stimulus
• Rotated by 90°
– Sensory epithelia not aligned
– Respond differently to a given stimulus
Transplantation Results
Ear Removed 3 Ears Normal 3 Ears Rotated Normal Rotated
Swimming was most affected when ear was removed or when 3rd ear was rotated
3 ears, all normal orientation 3 ears, one rotated 90°
1 ear 2 ears, Normal orientation
Afferent innervation depends upon orientation
Normal Orientation Rotated by 90°
Single z-series Images Single z-series Images
Animal A Animal B Animal C Animal D
• Lipophilic dye-soaked filter paper was injected into native (red) and transplanted ears (blue, false colored green)
• Brain removed and sensory
neurons were imaged with confocal microscope
• Single optical sections were
observed
Loss of input or gain of input affected dendritic branching of target neurons
• Dendritic development of brain neurons depends upon neuronal input – Loss of input (no ear) results in reduced branching – Gain of input (extra ear) results in increased branching
• Blocking afferent activity does not affect dendritic branching
(Goodman and Model, 1990), therefore branching is independent of the ear’s orientation
Proposed Mechanism
Normal Rotated
Testing the mechanism: Determine whether ear manipulations affect initial direction of movement
Conclusions
• Sensory neurons of transplanted ears rotated 90° interfere with vestibular processing as indicated by the aberrant swimming, similar to that of one-eared frogs.
• Partial overlap and segregation of sensory neurons implies that differential gravity sensation affects guidance of afferent axons in addition to molecular mechanisms.
• Altered sensory neuron input affects the dendritic branching of target neurons, such as the Mauthner cell.
Future Directions
• Alter gravity using a ‘frog elevator’
– Simulated parabolic flight
http://umps.med.univ-tours.fr/images/eng_parabole1.jpg
0g 2g 0g 2g
Acknowledgements
• Bernd Fritzsch
• Israt Jahan
• Ning Pan
• Tian Yang
• Jennifer Kersigo
• Ryan Ries
• Jeremy Duncan
• Ben Kopecky
• Hannah Maher
• Alex Perk
• Dr. Douglas Houston
• Dr. James Buchholz
• Dr. Dan Weeks
• Funding – NASA base grant
– NIH
– Iowa Center for Molecular Auditory Neuroscience