Functional and ultrastructural analysis of reafferent mechanosensation in larval zebrafish

Abstract

All animals need to differentiate between exafferent stimuli, which are caused by the environment, and reafferent stimuli, which are caused by their own movement. In the case of mechanosensation in aquatic animals, the exafferent inputs are water vibrations in the animal’s proximity, which need to be distinguished from the reafferent inputs arising from fluid drag due to locomotion. Both of these inputs are detected by the lateral line, a collection of mechanosensory organs distributed along the surface of the body.In this study, we characterize in detail how the hair cells, which are the receptor cells of the lateral line, discriminate between such reafferent and exafferent signals in zebrafish larvae. Using dye labeling of the lateral line nerve, we visualize two parallel descending inputs that can influence lateral line sensitivity. We combine functional imaging with ultra-structural EM circuit reconstruction to show that cholinergic signals originating from the hindbrain transmit efference copies that cancel out self-generated reafferent stimulation during locomotion, and that dopaminergic signals from the hypothalamus may have a role in threshold modulation both in response to locomotion and salient stimuli. We further gain direct mechanistic insight into the core components of this circuit by loss-of-function perturbations using targeted ablations and gene knockouts.We propose that this simple circuit is the core implementation of mechanosensory reafferent suppression in these young animals and that it might form the first instantiation of state-dependent modulation found at later stages in development.

Epigenetically distinct synaptic architecture in clonal compartments in the teleostean dorsal pallium

“…Here, it should be noted that our axonal projection analysis might have missed the projections from mature neurons, because the HuC promoter labels preferentially neural progenitors and disappears at later stages 19 . Thus, brain-wide exhaustive connectome analysis by electron microscopy 42 or neurophysiological analysis will be necessary for further study 43 .…”

Automated synapse-level reconstruction of neural circuits in the larval zebrafish brain

“…Also, manual reconstructions of connectivity are labor-intensive and costly. Thus, with the exception of the olfactory bulb work mentioned above 11,13 , EM-based circuit analysis in zebrafish has been limited to few cells in specific areas of the nervous system 10,[17][18][19][20][21] . One of our aims is to make connectomic data and computational tools available to the entire zebrafish community.…”

Locomotion-induced ocular motor behavior in larval Xenopus is developmentally tuned by visuo-vestibular reflexes

“…So far, eye movements triggered by lateral line stimulation have not been demonstrated. However, the common synaptic input of ascending locomotor efference copy pathways to both, vestibular and lateral line efferent neurons 45,46 , suggests that the two sensory systems might also share common motor targets such as extraocular motoneurons.…”