Cell-type-specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Proc Natl Acad Sci U S A. 2017 Sep 5;114(36):E7612-E7621. doi: 10.1073/pnas.1704893114. Epub 2017 Aug 21.

Abstract

Striatal spiny projection neurons (SPNs) receive convergent excitatory synaptic inputs from the cortex and thalamus. Activation of spatially clustered and temporally synchronized excitatory inputs at the distal dendrites could trigger plateau potentials in SPNs. Such supralinear synaptic integration is crucial for dendritic computation. However, how plateau potentials interact with subsequent excitatory and inhibitory synaptic inputs remains unknown. By combining computational simulation, two-photon imaging, optogenetics, and dual-color uncaging of glutamate and GABA, we demonstrate that plateau potentials can broaden the spatiotemporal window for integrating excitatory inputs and promote spiking. The temporal window of spiking can be delicately controlled by GABAergic inhibition in a cell-type-specific manner. This subtle inhibitory control of plateau potential depends on the location and kinetics of the GABAergic inputs and is achieved by the balance between relief and reestablishment of NMDA receptor Mg2+ block. These findings represent a mechanism for controlling spatiotemporal synaptic integration in SPNs.

Keywords: dendritic computation; inhibition; plateau potential; striatum; synaptic integration.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / physiology
  • Dendrites / metabolism
  • Dendrites / physiology*
  • Excitatory Postsynaptic Potentials / physiology*
  • Female
  • Glutamic Acid / metabolism
  • Male
  • Mice
  • Neural Pathways / metabolism
  • Neural Pathways / physiology
  • Neurons / metabolism
  • Neurons / physiology*
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Synapses / metabolism
  • Synapses / physiology
  • Synaptic Transmission / physiology
  • Thalamus / metabolism
  • Thalamus / physiology
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Receptors, N-Methyl-D-Aspartate
  • Glutamic Acid
  • gamma-Aminobutyric Acid