Conservation of locomotion-induced oculomotor activity through evolution in mammals

Barros, Filipa França de; Bacqué-Cazenave, Julien; Taillebuis, Coralie; Courtand, Gilles; Manuel, Marin; Bras, Hélène; Tagliabue, Michele; Combes, Denis; Lambert, François; Beraneck, Mathieu

doi:10.1016/j.cub.2021.11.022

Cited by 14 publications

(7 citation statements)

References 35 publications

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“…Significantly, this gaze-stabilizing mechanism that relies on locomotor EC signaling is not merely idiosyncratic to amphibians with their simpler and more stereotyped locomotor movement profiles, but evidently is also employed by other vertebrates, including humans. Recent studies in both Xenopus and mice (França de Barros et al, 2021;Bacqué-Cazenave et al, 2022) suggest that locomotor ECs can be used differently across species, depending on the biomechanical properties of their propulsive systems, their body organization, and the complexity of the sensory reference frames used to detect effective motion in space (Figure 6). This mechanism therefore represents an appealing example of a fundamental neural computation process that emerged early during vertebrate evolution and which was subsequently preserved, although necessarily superimposed by additional integrative mechanisms that accompanied the phylogenetic increase in sensory and motor system complexity.…”

Section: Discussionmentioning

confidence: 99%

“…More direct evidence for locomotor EC-driven eye movements has recently been discovered in mice, where the existence of a comparable spino-ocular motor coupling has been established by multi-methodological approaches (França de Barros et al, 2021). Briefly, ocular motor activity remaining strictly phase-coupled to the rhythm of fictive locomotion was encountered in ex vivo brain-spinal cord preparations of neonatal mice with spatio-temporal characteristics reminiscent of those described in Xenopus.…”

Section: Evolution and Ubiquity Of Locomotor Efference Copy-driven Ga...mentioning

confidence: 99%

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Role of locomotor efference copy in vertebrate gaze stabilization

Lambert¹,

Simmers²

2022

Front. Neural Circuits

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Vertebrate locomotion presents a major challenge for maintaining visual acuity due to head movements resulting from the intimate biomechanical coupling with the propulsive musculoskeletal system. Retinal image stabilization has been traditionally ascribed to the transformation of motion-related sensory feedback into counteracting ocular motor commands. However, extensive exploration of spontaneously active semi-intact and isolated brain/spinal cord preparations of the amphibian Xenopus laevis, have revealed that efference copies (ECs) of the spinal motor program that generates axial- or limb-based propulsion directly drive compensatory eye movements. During fictive locomotion in larvae, ascending ECs from rostral spinal central pattern generating (CPG) circuitry are relayed through a defined ascending pathway to the mid- and hindbrain ocular motor nuclei to produce conjugate eye rotations during tail-based undulatory swimming in the intact animal. In post-metamorphic adult frogs, this spinal rhythmic command switches to a bilaterally-synchronous burst pattern that is appropriate for generating convergent eye movements required for maintaining image stability during limb kick-based rectilinear forward propulsion. The transition between these two fundamentally different coupling patterns is underpinned by the emergence of altered trajectories in spino-ocular motor coupling pathways that occur gradually during metamorphosis, providing a goal-specific, morpho-functional plasticity that ensures retinal image stability irrespective of locomotor mode. Although the functional impact of predictive ECs produced by the locomotory CPG matches the spatio-temporal specificity of reactive sensory-motor responses, rather than contributing additively to image stabilization, horizontal vestibulo-ocular reflexes (VORs) are selectively suppressed during intense locomotor CPG activity. This is achieved at least in part by an EC-mediated attenuation of mechano-electrical encoding at the vestibular sensory periphery. Thus, locomotor ECs and their potential suppressive impact on vestibular sensory-motor processing, both of which have now been reported in other vertebrates including humans, appear to play an important role in the maintenance of stable vision during active body displacements.

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Section: Discussionmentioning

confidence: 99%

Section: Evolution and Ubiquity Of Locomotor Efference Copy-driven Ga...mentioning

confidence: 99%

Role of locomotor efference copy in vertebrate gaze stabilization

Lambert¹,

Simmers²

2022

Front. Neural Circuits

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“…Efference copies and corollary discharge signals have been shown to influence sensory processing in a variety of different systems and at different levels culminating in the predictive coding hypothesis (Combes et al, 2008; Crapse and Sommer, 2008; França de Barros et al, 2022; Fukutomi and Carlson, 2020; Poulet and Hedwig, 2006; Sommer and Wurtz, 2008; Wurtz, 2008). Despite decades of research, the mechanisms underlying the action of efference copies remain largely speculative.…”

Section: Discussionmentioning

confidence: 99%

Multiple mechanisms mediate the suppression of motion vision during escape maneuvers in flying Drosophila

Fischer¹,

Schnell²

2022

Preprint

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Animals must be able to discriminate self-generated (reafferent) from external (exafferent) sensory input. Otherwise, the former could interfere with perception and behavioral actions. The way this can be achieved is through an efference copy, which suppresses reafferent sensory input. An example for this is the optomotor response of the fly. With the optomotor response, flies stabilize a straight flight path by correcting for unintended deviations, which they sense as visual motion of their surrounding or optic flow. HS cells of the fly are tuned to rotational optic flow and are thought to mediate optomotor responses to horizontal motion. It has been shown that during spontaneous turns, an efference copy influences the membrane potential of HS cells. Here we investigate the influence of an efference copy during looming-elicited evasive turns combined with a subsequent optomotor stimulus in Drosophila. We show that looming stimuli themselves can influence the processing of preferred-direction motion in HS cells. In addition, an efference copy can influence visual processing during saccades in both directions, but only in a subset of cells. Our study supports the notion that processing of sensory information is finely tuned and dependent on both stimulus history and behavioral context.

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“…Ethologists and neuro-ethologists compare behaviors, MPs, and CPGs to understand the evolutionary mechanism(s) underlying one or several activities [ 55 ]. Functional morphologists compare “kinematics” (e.g., profiles and performances), and behavioral MPs to understand the links between “form” and “function” associated with one or more behaviors (e.g., functional trade-off) [ 56 , 57 , 58 , 59 ].…”

Section: Core Concept Of Neuroethological Morphologymentioning

confidence: 99%

Studies of the Behavioral Sequences: The Neuroethological Morphology Concept Crossing Ethology and Functional Morphology

Bels

Pallandre

Pellé

et al. 2022

Animals

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Postures and movements have been one of the major modes of human expression for understanding and depicting organisms in their environment. In ethology, behavioral sequence analysis is a relevant method to describe animal behavior and to answer Tinbergen’s four questions testing the causes of development, mechanism, adaptation, and evolution of behaviors. In functional morphology (and in biomechanics), the analysis of behavioral sequences establishes the motor pattern and opens the discussion on the links between “form” and “function”. We propose here the concept of neuroethological morphology in order to build a holistic framework for understanding animal behavior. This concept integrates ethology with functional morphology, and physics. Over the past hundred years, parallel developments in both disciplines have been rooted in the study of the sequential organization of animal behavior. This concept allows for testing genetic, epigenetic, and evo-devo predictions of phenotypic traits between structures, performances, behavior, and fitness in response to environmental constraints. Based on a review of the literature, we illustrate this concept with two behavioral cases: (i) capture behavior in squamates, and (ii) the ritualistic throat display in lizards.

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Conservation of locomotion-induced oculomotor activity through evolution in mammals

Cited by 14 publications

References 35 publications

Role of locomotor efference copy in vertebrate gaze stabilization

Role of locomotor efference copy in vertebrate gaze stabilization

Multiple mechanisms mediate the suppression of motion vision during escape maneuvers in flying Drosophila

Studies of the Behavioral Sequences: The Neuroethological Morphology Concept Crossing Ethology and Functional Morphology

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