Straka H et al. (2022), Role of locomotor efference copy in vertebrate ...

XB-ART-59671

Front Neural Circuits 2022 Jan 01;16:1040070. doi: 10.3389/fncir.2022.1040070.

Show Gene links Show Anatomy links

Role of locomotor efference copy in vertebrate gaze stabilization.

Straka H , Lambert FM , Simmers J .

???displayArticle.abstract???
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.

???displayArticle.pubmedLink??? 36569798
???displayArticle.pmcLink??? PMC9780284
???displayArticle.link??? Front Neural Circuits

Species referenced: Xenopus laevis
GO keywords: locomotory behavior [+]

???attribute.lit??? ???displayArticles.show???

	Figure 1. Schematic of central pathways responsible for the transformation of head/body motion-related sensory signals (from visual motion, vestibular endorgans, neck proprioceptors) and ascending motor efference copies (ECs) from spinal locomotor CPG networks into ocular motor commands for gaze stabilization during tail undulatory swimming in Xenopus larvae (bottom left) and limb-kicking propulsion in adults (bottom right).
	Figure 2. Semi-intact preparation of Xenopus larvae for studying the influence of spinal motor network ECs in gaze stabilization during fictive locomotion. (A1–5) Schematic of a head-brainstem-spinal cord preparation (A1) depicting recordings (A2) of a left and right spinal ventral root (Vr, blue traces), a synergistic left lateral rectus (LR, orange trace) and a right medial rectus (MR, red trace) extraocular motor nerve; direct spino-ocular motor connectivity (A3) conveys a copy of swimming motor output from the spinal CPG circuitry to drive compensatory conjugate eye movements during head movements resulting from propulsive bending (A4), mainly of the mid-tail region [indicated by color intensity grading in panel (A5)]. (B1,2) Schematics of the isolated central nervous system (B1) illustrating various surgical lesions and drug application interventions that allowed identifying the ascending pathway from the spinal CPG circuitry to bilateral synergistic sets of LR and MR extraocular motoneurons; 1, 2, disconnection of the midbrain [1 in panel (B1)] and cerebellum [2 in panel (B1)]; 3, hemisection of the brainstem/spinal cord at the level of the obex on the side ipsilateral to a recorded (left) LR nerve (B2) whose burst activity occurred in phase with Vr bursts on the opposite (right) cord side; 4, longitudinal midline split throughout the first 10 spinal segments (B1); 5, injection of glutamatergic transmitter antagonists (CNQX + KYNA) into the vestibular nucleus to block central processing of sensory endorgan signals (B2); 6, midline incision at the level of the abducens nucleus in rhombomere 5 (B2). These interventions and their respective effects on spino-ocular motor coupling to the synergistic left LR and right MR nerves are summarized in the table at right.
	Figure 3. Neuronal pathways underlying spino-ocular motor coupling during swimming in pre- and post-metamorphic Xenopus. (A) Schematic depicting the spinal CPG for tail-based propulsion in larvae and pathway connections that convey spinal EC signals to the extraocular motor system; after crossing the spinal cord, ascending projections from the spinal axial CPG network directly drive abducens motoneurons (Abd MN) innervating the lateral rectus (LR) eye muscle on the opposite side and indirectly via abducens internuclear neurons (Abd IN) drive oculomotor motoneurons (Oc MN) innervating the synergistic medial rectus (MR) eye muscle on the same side; this spino-ocular connectivity produces conjugate eye movements during swimming. (B) Schematic depicting the spinal CPG for limb-based rectilinear forward propulsion in juvenile Xenopus and pathway connections with the extraocular motor system; ascending, uncrossed projections from the spinal appendicular locomotor network activate ipsilateral Abd MNs and Oc MNs to produce convergent eye movements during each hindlimb extensor-driven kick cycle. (C) During metamorphic climax, larval and adult CPG circuits co-exist and can be conjointly active, producing a combination of tail- and limb-based propulsion and corresponding EC signals that continuously elicit appropriate conjugate and convergent eye movements; the influence of the appendicular system on ocular motor control progressively increases as the impact of the axial system declines as limb-based locomotion emerges, co-exists with, and eventually replaces tail-based locomotion during metamorphosis (schematized at bottom).
	Figure 4. Differential swim intensity-dependent interactions between vestibular sensory signals and locomotor ECs. (A) Schematic depicting the gating of vestibulo-ocular signaling during intense swimming in older larvae or in rapidly-swimming young larvae, leading to ocular motor performance remaining coordinated with tail undulations exclusively through an ascending drive from spinal ECs; during less intense or slow swimming (B), ocular motor performance results from an additive relationship between the predictive ECs and horizontal semicircular canal signals, with the latter now contributing significantly to compensatory eye motion; the two processing configurations gradually change their respective dominance depending on swimming strength and frequency (bottom schematic). Abd, abducens motoneurons; CPG, central pattern generator; VOR, vestibulo-ocular reflex; VS, vestibulo-spinal pathway.
	Figure 5. Attenuation of mechanosensory signal encoding in the inner ear during locomotor activity in larval Xenopus. (A) Summary schematic of the circuit elements mediating the vestibulo-ocular reflex (VOR), spino-ocular motor coupling and activation of inner ear vestibular efferent neurons (Vest. eff.) by locomotor ECs. (B) Influence of locomotor activity conveyed by Vest. eff. onto hair cells and vestibular afferent neurons (Vest. aff.); during swimming (right), the overall responsiveness of vest. aff. (magnitude of the sine wave) to imposed cyclic head rotation is substantially reduced compared to the condition without swimming (left). Abd MN, abducens motoneurons; Vr, spinal ventral root.
	Figure 6. Hypothetical evolutionary development of locomotor complexity in vertebrates, the accompanying increase in morphological complexity and the role played by vestibular sensory signaling, and the resultant gradual decline in locomotor EC influence in the production of compensatory eye movements. Despite the increasing capability of inner ear endorgans for motion detection and sensory-motor transformations, locomotor EC signals appear to have maintained an important role in gaze stabilization, even during bipedal locomotion.

References [+] :

Angelaki, Vestibular system: the many facets of a multimodal sense. 2008, Pubmed