Gaze Stabilization by Efference Copy Signaling without Sensory Feedback during Vertebrate Locomotion

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 compensa...

Full description

Saved in:
Bibliographic Details
Published in:Current biology 2012-09, Vol.22 (18), p.1649-1658
Main Authors: Lambert, François M., Combes, Denis, Simmers, John, Straka, Hans
Format: Article
Language:English
Subjects:
Animals
Eye Movements
eyes
Feedback, Sensory
Fixation, Ocular
frogs
head
Head Movements
Life Sciences
locomotion
Reflex, Vestibulo-Ocular
Reflex, Vestibulo-Ocular - physiology
reflexes
Saccades
Signal Transduction
spinal cord
Swimming
Swimming - physiology
tadpoles
Xenopus
Xenopus laevis
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
Description
Summary: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. 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. 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. ► A novel feedforward mechanism for gaze stabilization during vertebrate locomotion ► Locomotor efference copy drives compensatory eye movements in larval frogs ► The intrinsic CPG signals are conveyed directly to the extraocular motor nuclei ► The efference copy supersedes, rather than supplements, vestibulo-ocular reflexes
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2012.07.019