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Fast synaptic transmission between striatal spiny projection neurons

  1. Dietmar Plenz*‡
  1. *Unit of Neural Network Physiology, Laboratory of Systems Neuroscience, National Institute of Mental Health, 9000 Rockville Pike, Bethesda, MD 20892; and †Department of Anatomy and Neurobiology, University of Tennessee College of Medicine, 875 Monroe Avenue, Memphis, TN 38163

  1. Edited by Ann M. Graybiel, Massachusetts Institute of Technology, Cambridge, MA, and approved October 2, 2002 (received for review July 18, 2002)

Abstract

Striatal inhibition plays an important role in models of cortex-basal ganglia function and is altered in many basal ganglia diseases. The γ-aminobutyric acid ergic spiny projection neuron comprises >95% of striatal neurons, but despite strong anatomical evidence, the electrophysiological properties and functions of their local axon collaterals are unknown. We simultaneously recorded from adjacent spiny projection neurons (<5–10 μm) in whole-cell patch mode and demonstrated a fast synaptic connection between 26/69 pairs in cortex-striatum-substantia nigra organotypic cultures and 5/38 pairs in acute striatal slices. The synapse, which was blocked by γ-aminobutyric acid type A antagonists, displayed a wide range of failure rates, was depolarizing at rest, and reversed above −60 mV. Presynaptic bursts of action potentials were highly correlated with total postsynaptic depolarization at rest. Synaptic transmission was optimized for burst discharge >14 Hz and showed considerable short-term plasticity, including paired-pulse depression at intervals <25 ms, intraburst facilitation, and interburst augmentation. This activity-dependent collateral interaction provides the basis for a new class of basal ganglia models in which striatal neurons cooperate as well as compete during processing of cortical inputs.

Footnotes

    • ↵‡ To whom correspondence should be addressed. E-mail: plenzd{at}intra.nimh.nih.gov.

    • This paper was submitted directly (Track II) to the PNAS office.

  • Abbreviations

    • GABA, γ-aminobutyric acid

    • VRest, resting membrane potential

    • PSP, postsynaptic potential

    • Received July 18, 2002.

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