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The Journal of Neuroscience, August 6, 2008, 28(32):8086-8095; doi:10.1523/JNEUROSCI.1288-08.2008
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Behavioral/Systems/Cognitive
Semicircular Canal Size Determines the Developmental Onset of Angular Vestibuloocular Reflexes in Larval Xenopus
François M. Lambert,1,2 * James C. Beck,2,3 * Robert Baker,2 andHans Straka1 1Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7060, Université Paris Descartes, 75270 Paris Cedex 06, France, 2Department of Physiology and Neuroscience, New York University School of Medicine, New York, New York 10016, and 3Department of Biology, Long Island University, Brooklyn, New York 11201
Correspondence should be addressed to Dr. Hans Straka, Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7060, Université Paris Descartes, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France. Email: hans.straka{at}univ-paris5.fr
Semicircular canals have been sensors of angular acceleration for 450 million years. This vertebrate adaptation enhances survival by implementing postural and visual stabilization during motion in a three-dimensional environment. We used an integrated neuroethological approach in larval Xenopus to demonstrate that semicircular canal dimensions, and not the function of other elements, determines the onset of angular acceleration detection. Before angular vestibuloocular function in either the vertical or horizontal planes, at stages 47 and 48, respectively, each individual component of the vestibuloocular system was shown to be operational: extraocular muscles could be activated, central neural pathways were complete, and canal hair cells were capable of evoking graded responses. For Xenopus, a minimum semicircular canal lumen radius of 60 µm was necessary to permit endolymph displacement sufficient for sensor function at peak accelerations of 400°/s2. An intra-animal comparison demonstrated that this size is reached in the vertical canals earlier in development than in the horizontal canals, corresponding to the earlier onset of vertical canal-activated ocular motor behavior. Because size constitutes a biophysical threshold for canal-evoked behavior in other vertebrates, such as zebrafish, we suggest that the semicircular canal lumen and canal circuit radius are limiting the onset of vestibular function in all small vertebrates. Given that the onset of gravitoinertial acceleration detection precedes angular acceleration detection by up to 10 d in Xenopus, these results question how the known precise spatial patterning of utricular and canal afferents in adults is achieved during development.
Key words: vestibular; vestibuloocular reflex; otolith; zebrafish; development; extraocular
Received March 26, 2008; revised June 30, 2008; accepted July 2, 2008.
Correspondence should be addressed to Dr. Hans Straka, Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7060, Université Paris Descartes, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France. Email: hans.straka{at}univ-paris5.fr
This article has been cited by other articles:
M. Beraneck and F. M. Lambert
Impaired Perception of Gravity Leads to Altered Head Direction Signals: What Can We Learn From Vestibular-Deficient Mice?
J Neurophysiol, July 1, 2009; 102(1): 12 - 14.
[Abstract] [Full Text] [PDF]
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