Predictability of visual perturbation during locomotion: implications for corrective efference copy signaling.
Abstract: In guiding adaptive behavior, efference copy signals or corollary discharge are traditionally considered to serve as predictors of self-generated sensory inputs and by interfering with their central processing are able to counter unwanted consequences of an animal's own actions. Here, in a speculative reflection on this issue, we consider a different functional role for such intrinsic predictive signaling, namely in stabilizing gaze during locomotion where resultant changes in head orientation in space require online compensatory eye movements in order to prevent retinal image slip. The direct activation of extraocular motoneurons by locomotor-related efference copies offers a prospective substrate for assisting self-motion derived sensory feedback, rather than being subtracted from the sensory signal to eliminate unwanted reafferent information. However, implementing such a feed-forward mechanism would be critically dependent on an appropriate phase coupling between rhythmic propulsive movement and resultant head/visual image displacement. We used video analyzes of actual locomotor behavior and basic theoretical modeling to evaluate head motion during stable locomotion in animals as diverse as Xenopus laevis tadpoles, teleost fish and horses in order to assess the potential suitability of spinal efference copies to the stabilization of gaze during locomotion. In all three species, and therefore regardless of aquatic or terrestrial environment, the head displacements that accompanied locomotor action displayed a strong correlative spatio-temporal relationship in correspondence with a potential predictive value for compensatory eye adjustments. Although spinal central pattern generator-derived efference copies offer appropriately timed commands for extraocular motor control during self-generated motion, it is likely that precise image stabilization requires the additional contributions of sensory feedback signals. Nonetheless, the predictability of the visual consequences of stereotyped locomotion renders intrinsic efference copy signaling an appealing mechanism for offsetting these disturbances, thus questioning the exclusive role traditionally ascribed to sensory-motor transformations in stabilizing gaze during vertebrate locomotion.
Publication Date: 2012-11-20 PubMed ID: 23179256DOI: 10.1007/s00422-012-0528-0Google Scholar: Lookup
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Summary
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The research paper explores efference copy signals’ role as predictive mechanisms, which traditionally counter ill effects of an organism’s actions by influencing the processing of self-generated inputs. The study suggests another prospective function—for stabilizing gaze during locomotion—in varying species like Xenopus laevis tadpoles, teleost fish, and horses. While the role of these signals in compensating for eye movements is speculated, sensory feedback signals are likely crucial for exact image stabilization.
Efference Copy Signals
- The traditional view assigns an anticipatory role to efference copy signals. These signals are believed to predict self-generated inputs, interfacing with their central processing to combat the undesired effects of an animal’s actions.
- This research proposes a different role for these signals—as a stabilizing agent during locomotion, particularly for gaze. Changes in head orientation require compensatory eye movements, and efference copy signals could aid in maintaining stability.
Role in Locomotion
- The possibility of extraocular motoneurons being directly activated by locomotor-related efference copies provides the basis for this idea. This suggests that efference copy signals might act to assist sensory feedback derived from self-motion rather than being a subtractive agent from the sensory signal for eliminating unwanted reafferent information.
- However, the practicality of such a mechanism would depend on the precise phase relationship between the propulsive movement and the resultant displacement of the head/visual image.
Data Evaluation and Analysis
- The researchers used video analysis and theoretical modeling to examine locomotion in three different species—Xenopus laevis tadpoles, teleost fish, and horses.
- Regardless of the animals’ different environments, there was a strong spatial-temporal correlation between head movements and locomotor action, suggesting a potential predictive value for compensatory eye adjustments.
Concluding Remarks
- The paper suggests that while spinal central pattern generator-derived efference copies could provide accurately timed commands for eye motor control during self-generated motion, accurate image stabilization would likely need extra sensory feedback signals.
- However, the predictability of visual disturbances during standard locomotion opens up the potential importance of intrinsic efference copy signals in negating these interferences.
- This research challenges the traditional view of sensory-motor transformations’ exclusive role in stabilizing gaze during vertebrate locomotion.
Cite This Article
APA
Chagnaud BP, Simmers J, Straka H.
(2012).
Predictability of visual perturbation during locomotion: implications for corrective efference copy signaling.
Biol Cybern, 106(11-12), 669-679.
https://doi.org/10.1007/s00422-012-0528-0 Publication
Researcher Affiliations
- Department Biology II, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Munich, Germany. b.chagnaud@gmail.com
MeSH Terms
- Adaptation, Psychological / physiology
- Animals
- Eye Movements / physiology
- Feedback, Sensory / physiology
- Head Movements
- Humans
- Locomotion / physiology
- Models, Biological
- Predictive Value of Tests
- Spinal Cord / physiology
- Vestibule, Labyrinth / physiology
Citations
This article has been cited 13 times.- Straka H, Lambert FM, Simmers J. Role of locomotor efference copy in vertebrate gaze stabilization.. Front Neural Circuits 2022;16:1040070.
- Dietrich H, Pradhan C, Heidger F, Schniepp R, Wuehr M. Downbeat nystagmus becomes attenuated during walking compared to standing.. J Neurol 2022 Dec;269(12):6222-6227.
- Latash ML. Efference copy in kinesthetic perception: a copy of what is it?. J Neurophysiol 2021 Apr 1;125(4):1079-1094.
- Meshida K, Lin S, Domning DP, Wang P, Gilland E. The oblique extraocular muscles in cetaceans: Overall architecture and accessory insertions.. J Anat 2021 Apr;238(4):917-941.
- Fukutomi M, Carlson BA. A History of Corollary Discharge: Contributions of Mormyrid Weakly Electric Fish.. Front Integr Neurosci 2020;14:42.
- Dietrich H, Heidger F, Schniepp R, MacNeilage PR, Glasauer S, Wuehr M. Head motion predictability explains activity-dependent suppression of vestibular balance control.. Sci Rep 2020 Jan 20;10(1):668.
- Dietrich H, Wuehr M. Selective suppression of the vestibulo-ocular reflex during human locomotion.. J Neurol 2019 Sep;266(Suppl 1):101-107.
- MacNeilage PR, Glasauer S. Quantification of Head Movement Predictability and Implications for Suppression of Vestibular Input during Locomotion.. Front Comput Neurosci 2017;11:47.
- Straka H, Chagnaud BP. Moving or being moved: that makes a difference.. J Neurol 2017 Oct;264(Suppl 1):28-33.
- Branoner F, Chagnaud BP, Straka H. Ontogenetic Development of Vestibulo-Ocular Reflexes in Amphibians.. Front Neural Circuits 2016;10:91.
- Chagnaud BP, Banchi R, Simmers J, Straka H. Spinal corollary discharge modulates motion sensing during vertebrate locomotion.. Nat Commun 2015 Sep 4;6:7982.
- Fritzsch B, Straka H. Evolution of vertebrate mechanosensory hair cells and inner ears: toward identifying stimuli that select mutation driven altered morphologies.. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2014 Jan;200(1):5-18.
- von Uckermann G, Le Ray D, Combes D, Straka H, Simmers J. Spinal efference copy signaling and gaze stabilization during locomotion in juvenile Xenopus frogs.. J Neurosci 2013 Mar 6;33(10):4253-64.
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