Gaze stabilization by efference copy signaling without sensory feedback during vertebrate locomotion.
Current Biology. 2012-09-01; 22(18): 1649-1658
DOI: 10.1016/j.cub.2012.07.019
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Lambert FM(1), Combes D, Simmers J, Straka H.
Author information:
(1)Centre d’Etudes de la SensoriMotricité, CNRS UMR 8194, Université Paris
Descartes, 45 rue des Saints-Pères, 75006 Paris, France.
Comment in
Nat Rev Neurosci. 2012 Sep;13(9):602.
Curr Biol. 2012 Sep 25;22(18):R796-7.
BACKGROUND: Self-generated body movements require compensatory eye and head
adjustments in order to avoid perturbation of visual information processing.
Retinal image stabilization is traditionally ascribed to the transformation of
visuovestibular signals into appropriate extraocular motor commands for
compensatory ocular movements. During locomotion, however, intrinsic “efference
copies” of the motor commands deriving from spinal central pattern generator
(CPG) activity potentially offer a reliable and rapid mechanism for image
stabilization, in addition to the slower contribution of movement-encoding
sensory inputs.
RESULTS: Using a variety of in vitro and in vivo preparations of Xenopus
tadpoles, we demonstrate that spinal locomotor CPG-derived efference copies do
indeed produce effective conjugate eye movements that counteract oppositely
directed horizontal head displacements during undulatory tail-based locomotion.
The efference copy transmission, by which the extraocular motor system becomes
functionally appropriated to the spinal cord, is mediated by direct ascending
pathways. Although the impact of the CPG feedforward commands matches the
spatiotemporal specificity of classical vestibulo-ocular responses, the two
fundamentally different signals do not contribute collectively to image
stabilization during swimming. Instead, when the CPG is active, horizontal
vestibulo-ocular reflexes resulting from head movements are selectively
suppressed.
CONCLUSIONS: These results therefore challenge our traditional understanding of
how animals offset the disruptive effects of propulsive body movements on visual
processing. Specifically, our finding that predictive efference copies of
intrinsic, rhythmic neural signals produced by the locomotory CPG supersede,
rather than supplement, reactive vestibulo-ocular reflexes in order to drive
image-stabilizing eye adjustments during larval frog swimming, represents a
hitherto unreported mechanism for vertebrate ocular motor control.
Copyright © 2012 Elsevier Ltd. All rights reserved.
DOI: 10.1016/j.cub.2012.07.019
PMID: 22840517 [Indexed for MEDLINE]