Excitatory and inhibitory synapses in neuropeptide Y-expressing striatal interneurons

J Neurophysiol. 2009 Nov;102(5):3038-45. doi: 10.1152/jn.00272.2009. Epub 2009 Sep 16.

Abstract

Although rare, interneurons are pivotal in governing striatal output by extensive axonal arborizations synapsing on medium spiny neurons. Using a genetically modified mouse strain in which a green fluorescent protein (GFP) is driven to be expressed under control of the neuropeptide Y (NPY) promoter, we identified NPY interneurons and compared them with striatal principal neurons. We found that the bacteria artificial chromosome (BAC)-npy mouse expresses GFP with high fidelity in the striatum to the endogenous expression of NPY. Patch-clamp analysis from NPY neurons showed a heterogeneous population of striatal interneurons. In the majority of cells, we observed spontaneous firing of action potentials in extracellular recordings. On membrane rupture, most NPY interneurons could be classified as low-threshold spiking interneurons and had high-input resistance. Voltage-clamp recordings showed that both GABA and glutamate gated ion channels mediate synaptic inputs onto these striatal interneurons. AMPA receptor-mediated spontaneous excitatory postsynaptic currents (sEPSCs) were small in amplitude and infrequent in NPY neurons. Evoked EPSCs did not show short-term plasticity but some rectification. Evoked N-methyl-d-aspartate (NMDA) EPSCs had fast decay kinetics and were poorly sensitive to an NR2B subunit containing NMDA receptor blocker. Spontaneous inhibitory postsynaptic currents (sIPSCs) were mediated by GABA(A) receptors and were quite similar among all striatal neurons studied. On the contrary, evoked IPSCs decayed faster in NPY neurons than in other striatal neurons. These data report for the first time specific properties of synaptic transmission to NPY striatal interneurons.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bicuculline / analogs & derivatives
  • Bicuculline / pharmacology
  • Biophysical Phenomena / drug effects
  • Biophysical Phenomena / physiology
  • Biophysics
  • Choline O-Acetyltransferase / metabolism
  • Corpus Striatum / cytology*
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • GABA Antagonists / pharmacology
  • Green Fluorescent Proteins / genetics
  • Interneurons / physiology*
  • Mice
  • Mice, Transgenic
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology*
  • Neuropeptide Y / genetics
  • Neuropeptide Y / metabolism*
  • Organophosphonates / pharmacology
  • Parvalbumins / metabolism
  • Patch-Clamp Techniques / methods
  • Piperazines / pharmacology
  • Quinoxalines / pharmacology
  • Sodium Channel Blockers / pharmacology
  • Synapses / drug effects
  • Synapses / physiology*
  • Synaptic Potentials / drug effects
  • Synaptic Potentials / physiology*
  • Tetrodotoxin / pharmacology

Substances

  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • Neuropeptide Y
  • Organophosphonates
  • Parvalbumins
  • Piperazines
  • Quinoxalines
  • Sodium Channel Blockers
  • carboxypiperazinyl propylphosphonic acid
  • 2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline
  • Green Fluorescent Proteins
  • Tetrodotoxin
  • bicuculline methobromide
  • Choline O-Acetyltransferase
  • Bicuculline