Activity patterns in the neuropil of striatal cholinergic interneurons in freely moving mice represent their collective spiking dynamics

Rotem Rehani, Yara Atamna, Lior Tiroshi, Wei Hua Chiu, José De Jesús Aceves Buendía, Gabriela J. Martins, Gilad A. Jacobson, Joshua A. Goldberg*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

Cholinergic interneurons (CINs) are believed to form synchronous cell assemblies that modulate the striatal microcircuitry and possibly orchestrate local dopamine release. We expressed GCaMP6s, a genetically encoded calcium indicator (GECIs), selectively in CINs, and used microendoscopes to visualize the putative CIN assemblies in the dorsal striatum of freely moving mice. The GECI fluorescence signal from the dorsal striatum was composed of signals from individual CIN somata that were engulfed by a widespread fluorescent neuropil. Bouts of synchronous activation of the cholinergic neuropil revealed patterns of activity that preceded the signal from individual somata. To investigate the nature of the neuropil signal and why it precedes the somatic signal, we target-patched GECI-expressing CINs in acute striatal slices in conjunction with multiphoton imaging or wide-field imaging that emulates the microendoscopes’ specifications. The ability to detect fluorescent transients associated with individual action potential was constrained by the long decay constant of GECIs (relative to common inorganic dyes) to slowly firing (<2 spikes/s) CINs. The microendoscopes’ resolving power and sampling rate further diminished this ability. Additionally, we found that only back-propagating action potentials but not synchronous optogenetic activation of thalamic inputs elicited observable calcium transients in CIN dendrites. Our data suggest that only bursts of CIN activity (but not their tonic firing) are visible using endoscopic imaging, and that the neuropil patterns are a physiological measure of the collective recurrent CIN network spiking activity.

Original languageAmerican English
Article numbere0351-18.2018
JournaleNeuro
Volume6
Issue number1
DOIs
StatePublished - 1 Jan 2019

Bibliographical note

Publisher Copyright:
© 2019 Rehani et al.

Keywords

  • Channelrhodopsin-2
  • Gradient reflective index (GRIN) lens
  • Local field potentials (LFPs)
  • Pacemaker
  • Spatiotemporal patterns
  • Two-photon laser scanning microscopy

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