Brainstem circuits encoding start, speed, and duration of swimming in adult zebrafish

Berg, Eva; Mrowka, Leander; Bertuzzi, Maria; Madrid, David; Picton, Laurence D.; Manira, Abdeljabbar El

doi:10.1016/j.neuron.2022.10.034

Cited by 35 publications

(20 citation statements)

References 80 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Similar to observations in the lamprey 10,51 , one parallel pathway likely involves a midbrain nucleus comprised of spinal-projecting neurons called the interstitial nucleus of Cajal, a.k.a. the nucleus of the medial longitudinal fasciculus (INC/nucMLF) 32,45,[52][53][54][55] . Vestibular information reaches the INC/nucMLF through ascending vestibular neurons in the tangential nucleus 32,42,54,56 .…”

Section: Discussionmentioning

confidence: 99%

The vestibulospinal nucleus is a locus of balance development

Hamling,

Harmon,

Kimura

et al. 2023

Preprint

View full text Add to dashboard Cite

Mature vertebrates maintain posture using vestibulospinal neurons that transform sensed instability into reflexive commands to spinal motor circuits. Postural stability improves across development. However, due to the complexity of terrestrial locomotion, vestibulospinal contributions to postural refinement in early life remain unexplored. Here we leveraged the relative simplicity of underwater locomotion to quantify the postural consequences of losing vestibulospinal neurons during development in larval zebrafish. By comparing posture at two timepoints, we discovered that later lesions of vestibulospinal neurons led to greater instability. Analysis of thousands of individual swim bouts revealed that lesions disrupted movement timing and corrective reflexes without impacting swim kinematics, particularly in older larvae. Using a generative model of swimming, we showed how these disruptions could account for the increased postural variability at both timepoints. Finally, late lesions disrupted the fin/trunk coordination observed in older larvae, linking vestibulospinal neurons to postural control schemes used to navigate in depth. Since later lesions were considerably more disruptive to postural stability, we conclude that vestibulospinal contributions to balance increase as larvae mature. Vestibulospinal neurons are highly conserved across vertebrates; we therefore propose that they are a substrate for developmental improvements to postural control.

show abstract

Section: Discussionmentioning

confidence: 99%

The vestibulospinal nucleus is a locus of balance development

Hamling,

Harmon,

Kimura

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…The neural basis of animal behavior, ranging from fast body movements to slow exploration-exploitation strategy, has been extensively studied in the literature (12,13,21,33,(49)(50)(51)(52)(53). The behavioral hierarchy (Fig.…”

Section: Discussionmentioning

confidence: 99%

Hierarchical behavior control by a single class of interneurons

Huo

Polat

et al. 2023

Preprint

View full text Add to dashboard Cite

Animal behavior is organized into nested temporal patterns spanning multiple timescales. This behavior hierarchy is believed to arise from a hierarchical neural architecture: neurons near the top of the hierarchy are involved in planning, selecting, initiating, and maintaining motor programs while those near the bottom of the hierarchy act in concert to produce fine spatiotemporal motor activity. InCaenorhabditis elegans, behavior on a long timescale emerges from ordered and flexible transitions between different behavioral states, such as forward movement, reversal, and turn. On a short timescale, different parts of the animal body coordinate fast rhythmic bending sequences to produce directional movements. Here, we show SAA, a class of interneurons that enable cross-communication between dorsal and ventral head motor neurons, play a dual role in shaping behavioral dynamics on different timescales. On the short timescale, SAA regulate and stabilize rhythmic bending activity during forward movements. On the long timescale, the same neurons suppress spontaneous reversals and facilitates reversal termination by inhibiting RIM, an integrating neuron that helps sustain a behavioral state. These results suggest that feedback from a lower-level cell assembly to a higher-level command center is essential for bridging behavioral dynamics at different levels.

show abstract

“…The nMLF is a vital component of the descending motor system, serving as a command center for forward locomotion [63][64][65][66][67][68][69][70]. The nMLF contains subpopulations of vGlut1 and vGlut2 positive neurons, which control both fast escape-swimming behaviors as well as slow forward locomotion [68,71]. Neurons in the nMLF were recently shown to respond to hindbrain cranial relay neurons (CRN; Fig 8A), which can be activated by aversive auditory stimulation of Mauthner cells, leading to smooth swimming after an initial C-bend response [63].…”

Section: Defective Sensorimotor Transformation In Vps4a T248i Mutantsmentioning

confidence: 99%

Defects in exosome biogenesis are associated with sensorimotor defects in zebrafishvps4amutants

Shipman,

Gao,

Liu

et al. 2024

Preprint

View full text Add to dashboard Cite

Mutations in humanVPS4Aare associated with neurodevelopmental defects, including motor delays and defective muscle tone.VPS4Aencodes a AAA-ATPase that is required for membrane scission, but how mutations inVPS4Alead to impaired control of motor function is not known. Here we identified a mutation in zebrafishvps4a, T248I, that affects sensorimotor transformation. In biochemical experiments we show that the T248I mutation reduces the ATPase activity of Vps4a and disassembly of its substrate, ESCRT filaments, which mediate membrane scission. Consistent with the established role for Vps4a in the endocytic pathway and exosome biogenesis,vps4aT248Imutants have enlarged endosomal compartments in the CNS and decreased numbers of circulating exosomes. Resembling the central form of hypotonia in humanVPS4Apatients, motor neurons and muscle cells are unaffected in mutant zebrafish as they react robustly to touch. Unlike somatosensory function, optomotor responses, vestibulospinal (VS), and acoustic startle reflexes are severely impaired invps4aT248Imutants, indicating a greater sensitivity of these circuits to the T248I mutation. ERG recordings indicate that visual ability is largely reduced in the mutants, however,in vivoimaging of tone-evoked responses in the inner ear and ascending auditory pathway show comparable activity. Further investigation of central pathways invps4aT248Imutants revealed that sensory cues failed to fully activate neurons in the VS and medial longitudinal fasciculus (MLF) nuclei that directly innervate motor neurons. Our results suggest that a defect in sensorimotor transformation underlies the profound yet selective effects on motor reflexes resulting from the loss of membrane scission mediated by Vps4a.

show abstract

Brainstem circuits encoding start, speed, and duration of swimming in adult zebrafish

Cited by 35 publications

References 80 publications

The vestibulospinal nucleus is a locus of balance development

The vestibulospinal nucleus is a locus of balance development

Hierarchical behavior control by a single class of interneurons

Defects in exosome biogenesis are associated with sensorimotor defects in zebrafishvps4amutants

Contact Info

Product

Resources

About