Rapid 3D Enhanced Resolution Microscopy Reveals Diversity in Dendritic Spinule Dynamics, Regulation, and Function

Colleen R. Zaccard, Lauren Shapiro, Maria D. Martin-de-Saavedra, Christopher Pratt, Kristoffer Myczek, Amy Song, Marc P. Forrest, Peter Penzes*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Dendritic spinules are thin protrusions, formed by neuronal spines, not adequately resolved by diffraction-limited light microscopy, which has limited our understanding of their behavior. Here we performed rapid structured illumination microscopy and enhanced resolution confocal microscopy to study spatiotemporal spinule dynamics in cortical pyramidal neurons. Spinules recurred at the same locations on mushroom spine heads. Most were short-lived, dynamic, exploratory, and originated near simple PSDs, whereas a subset was long-lived, elongated, and associated with complex PSDs. These subtypes were differentially regulated by Ca2+ transients. Furthermore, the postsynaptic Rac1-GEF kalirin-7 regulated spinule formation, elongation, and recurrence. Long-lived spinules often contained PSD fragments, contacted distal presynaptic terminals, and formed secondary synapses. NMDAR activation increased spinule number, length, and contact with distal presynaptic elements. Spinule subsets, dynamics, and recurrence were validated in cortical neurons of acute brain slices. Thus, we identified unique properties, regulatory mechanisms, and functions of spinule subtypes, supporting roles in neuronal connectivity.

Original languageEnglish (US)
Pages (from-to)522-537.e6
JournalNeuron
Volume107
Issue number3
DOIs
StatePublished - Aug 5 2020

Keywords

  • calcium transients
  • dendritic spine dynamics
  • intrabodies
  • kalirin-7
  • live imaging
  • multi-synaptic spines
  • postsynaptic density
  • structured illumination microscopy
  • synaptic plasticity
  • synaptic spinules

ASJC Scopus subject areas

  • Neuroscience(all)

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