Spatial patterning of excitatory and inhibitory neuropil territories during spinal circuit development

Qing Yan, Lu Zhai, Bo Zhang, Julia Dallman

Research output: Contribution to journalArticle

Abstract

To generate rhythmic motor behaviors, both single neurons and neural circuits require a balance between excitatory inputs that trigger action potentials and inhibitory inputs that promote a stable resting potential (E/I balance). Previous studies have focused on individual neurons and have shown that, over a short spatial scale, excitatory and inhibitory (E/I) synapses tend to form structured territories with inhibitory inputs enriched on cell bodies and proximal dendrites and excitatory inputs on distal dendrites. However, systems-level E/I patterns, at spatial scales larger than single neurons, are largely uncharted. We used immunostaining for PSD-95 and gephyrin postsynaptic scaffolding proteins as proxies for excitatory and inhibitory synapses, respectively, to quantify the numbers and map the distributions of E/I synapses in zebrafish spinal cord at both an embryonic stage and a larval stage. At the embryonic stage, we found that PSD-95 puncta outnumber gephyrin puncta, with the number of gephyrin puncta increasing to match that of PSD-95 puncta at the larval stage. At both stages, PSD-95 puncta are enriched in the most lateral neuropil corresponding to distal dendrites while gephyrin puncta are enriched on neuronal somata and in the medial neuropil. Significantly, similar to synaptic puncta, neuronal processes also exhibit medial-lateral territories at both developmental stages with enrichment of glutamatergic (excitatory) processes laterally and glycinergic (inhibitory) processes medially. This establishment of neuropil excitatory-inhibitory structure largely precedes dendritic arborization of primary motor neurons, suggesting that the structured neuropil could provide a framework for the development of E/I balance at the cellular level. J. Comp. Neurol. 525:1649–1667, 2017.

Original languageEnglish (US)
Pages (from-to)1649-1667
Number of pages19
JournalJournal of Comparative Neurology
Volume525
Issue number7
DOIs
StatePublished - May 1 2017

Fingerprint

Neuropil
Dendrites
Synapses
Neurons
Neuronal Plasticity
Carisoprodol
Motor Neurons
Proxy
Zebrafish
Membrane Potentials
Action Potentials
Spinal Cord
gephyrin
Proteins

Keywords

  • excitatory and inhibitory synapses
  • neuropil
  • RRID: AB141514
  • RRID: AB_2092365
  • RRID: AB_2534088
  • RRID: AB_2535773
  • RRID: AB_621842
  • RRID: AB_887717
  • RRID: nif-0000-00197
  • RRID: nif-0000-30467
  • RRID: nlx_153890
  • spinal cord
  • zebrafish

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Spatial patterning of excitatory and inhibitory neuropil territories during spinal circuit development. / Yan, Qing; Zhai, Lu; Zhang, Bo; Dallman, Julia.

In: Journal of Comparative Neurology, Vol. 525, No. 7, 01.05.2017, p. 1649-1667.

Research output: Contribution to journalArticle

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