Volume EM Reconstruction of Spinal Cord Reveals Wiring Specificity in Speed-Related Motor Circuits

Fabian N Svara,Jörgen Kornfeld,Winfried Denk,Johann H Bollmann

doi:10.1016/j.celrep.2018.05.023

Fabian N Svara, Jörgen Kornfeld + Show 2 more

Open Access

https://doi.org/10.1016/j.celrep.2018.05.023

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Journal: Cell Reports	Publication Date: Jun 1, 2018
Citations: 46	License type: cc-by

Affiliation: Max Planck Institute of Neurobiology

Abstract

Spinal interneurons coordinate the activity of motoneurons to generate the spatiotemporal patterns of muscle contractions required for vertebrate locomotion. It is controversial to what degree the orderly, gradual recruitment of motoneurons is determined by biophysical differences among them rather than by specific connections from presynaptic interneurons to subsets of motoneurons. To answer this question, we mapped all connections from two types of interneurons onto all motoneurons in a larval zebrafish spinal cord hemisegment, using serial block-face electron microscopy (SBEM). We found specific synaptic connectivity from dorsal but not from ventral excitatory ipsilateral interneurons, with large motoneurons, active only when strong force is required, receiving specific inputs from dorsally located interneurons, active only during fast swims. By contrast, the connectivity between inhibitory commissural interneurons and motoneurons lacks any discernible pattern. The wiring pattern is consistent with a recruitment mechanism that depends to a considerable extent on specific connectivity.

Highlights

Controlling the speed of locomotion requires controlling the frequency and force of rhythmic muscle contractions
Differential Patterns of circumferential descending INs (CiDs) IN and MN Recruitment In larval zebrafish, different CiD populations are active at different swim speeds (McLean et al, 2007, 2008)
In contrast to Ventral CiDs (V-CiDs), for which the activity decreases for swim speeds >40 Hz, the activity of MNs monotonically increases with swim speed

Summary

Introduction

Controlling the speed of locomotion requires controlling the frequency and force of rhythmic muscle contractions. In some cases the order of MN activation depends on how the behavior is elicited (Kanda et al, 1977), which is incompatible with a mechanism based only on an excitability gradient and instead suggests that at least some of the wiring is specific (Burke, 1979). This is further supported by recordings, made in zebrafish varying in age between juvenile and adult, showing that there are strong synaptic connections between interneurons (INs) and MNs that are recruited at similar speeds (Ampatzis et al, 2014; Song et al, 2016).

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Discussion

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