Locomotor corollary activation of trigeminal motoneurons: coupling of discrete motor behaviors

Abstract

During motor behavior, corollary discharges of the underlying motor commands inform sensory-motor systems about impending or ongoing movements. These signals generally limit the impact of self-generated sensory stimuli but also induce motor reactions that stabilize sensory perception. Here, we demonstrate in isolated preparations of Xenopus laevis tadpoles that locomotor corollary discharge provokes a retraction of the mechanoreceptive tentacles during fictive swimming. In the absence of sensory feedback, these signals activate a cluster of trigeminal motoneurons that cause a contraction of the tentacle muscle. This corollary discharge encodes duration and strength of locomotor activity, thereby ensuring a reliable coupling between locomotion and tentacle motion. The strict phase coupling between the trigeminal and spinal motor activity, present in many cases, suggests that the respective corollary discharge is causally related to the ongoing locomotor output and derives at least in part from the spinal central pattern generator; however, additional contributions from midbrain and/or hindbrain locomotor centers are likely. The swimming-related retraction might protect the touch-receptive Merkel cells on the tentacle from sensory over-stimulation and damage and/or reduce the hydrodynamic drag. The intrinsic nature of the coupling of tentacle retraction to locomotion is an excellent example of a context-dependent, direct link between otherwise discrete motor behaviors.

Efferent Modulation of Spontaneous Lateral Line Activity During and after Zebrafish Motor Commands

“…In order to survive, many animals must move across a wide range of speeds. In many aquatic animals an increased swimming frequency proportionally reduces afferent firing rate, likely due to the input of efferent neurons conveying this frequency information from active motor units (Russell 1971; Russell and Roberts 1972; Roberts and Russell 1972; Flock and Russell 1973; Hänzi et al 2015; Chagnaud et al 2015). In zebrafish, these speeds are achieved by increases in tail-beat frequency (Li et al 2012), which are generated in a tonotopic manner by shifts in activity by distinct groups of interneurons and motor neurons in the spinal cord (Mendell 2005; McLean et al 2007; McLean and Fetcho 2008).…”

A New Perspective on Predictive Motor Signaling

“…Another example of locomotor-to-motor coupling is found between the spinal swim-generating and hindbrain trigeminal motor circuitries that control movements of the paired mechanosensitive tentacles (similar to fish barbels) in Xenopus tadpoles [82]. A subset of trigeminal motoneurons, which receive spinal efference copy input about the duration, frequency and strength of ongoing locomotor movements, drive tentacle retractions that are likely to reduce the hydrodynamic resistance and/or prevent reafferent sensory stimulation of the tentacle during undulatory swimming movements [82]. Although yet to be established experimentally, other related examples of locomotor-to-motor coupling potentially mediated by efference copies include the retraction of limbs or external gills during the switch to undulatory tail-based swimming in the salamander and axolotl [83,84].…”

Ontogenetic Development of Vestibulo-Ocular Reflexes in Amphibians

“…(A–C) Visualization of the rhombomeric scaffold by either naturally occurring segmentally iterated accumulation of dark pigments in the center of the rhombomeres (A) , by labeling with streptavidin Alexa 546, outlining the rhombomeric boundaries (B) or by long wavelength illumination (633 nm) outlining midline-crossing fibers within each rhombomere (C) ; the material originates from brains of larval Rana clamitans ( A ; stage 26, according to Gosner, 1960) and Xenopus laevis ( B , with permission from Hänzi et al, 2015a; C , with permission from Chagnaud et al, 2015); images in (B,C) were obtained from tadpoles at stage 52 according to Nieuwkoop and Faber (1994). (D,E) Schematics depicting the segmental arrangement of spinal-projecting (green in D ), midbrain oculomotor nucleus-projecting (red in D ), vestibular commissural (orange in E ), and cerebellum-projecting neurons (blue in E ).…”

“…However, segments can also be visually defined by glial cell accumulation at the boundaries (Yoshida and Colman, 2000), by labeling with streptavidin Alexa 546 (Figure 5B; Hänzi et al, 2015a) or simply by illumination with a wavelength between 610–650 nm (Figure 5C; Chagnaud et al, 2015). These segments correspond to the rhombomeric scaffold described in Xenopus embryos (Papalopulu et al, 1991).…”