A Novel Functionally Distinct Subtype of Striatal Neuropeptide Y Interneuron

J Neurosci. 2011 Nov 16;31(46):16757-69. doi: 10.1523/JNEUROSCI.2628-11.2011.

Abstract

We investigated the properties of neostriatal neuropeptide Y (NPY)-expressing interneurons in transgenic GFP (green fluorescent protein)-NPY reporter mice. In vitro whole-cell recordings and biocytin staining demonstrated the existence of a novel class of neostriatal NPY-expressing GABAergic interneurons that exhibit electrophysiological, neurochemical, and morphological properties strikingly different from those of previously described NPY-containing, plateau-depolarization low-threshold spike (NPY-PLTS) interneurons. The novel NPY interneuron type (NPY-neurogliaform) differed from previously described NPY-PLTS interneurons by exhibiting a significantly lower input resistance and hyperpolarized membrane potential, regular, nonaccommodating spiking in response to depolarizing current injections, and an absence of plateau depolarizations or low-threshold spikes. NPY-neurogliaform interneurons were also easily distinguished morphologically by their dense, compact, and highly branched dendritic and local axonal arborizations that contrasted sharply with the sparse and extended axonal and dendritic arborizations of NPY-PLTS interneurons. Furthermore, NPY-neurogliaform interneurons did not express immunofluorescence for somatostatin or nitric oxide synthase that was ubiquitous in NPY-PLTS interneurons. IPSP/Cs could only rarely be elicited in spiny projection neurons (SPNs) in paired recordings with NPY-PLTS interneurons. In contrast, the probability of SPN innervation by NPY-neurogliaform interneurons was extremely high, the synapse very reliable (no failures were observed), and the resulting postsynaptic response was a slow, GABA(A) receptor-mediated IPSC that has not been previously described in striatum but that has been elicited from NPY-GABAergic neurogliaform interneurons in cortex and hippocampus. These properties suggest unique and distinctive roles for NPY-PLTS and NPY-neurogliaform interneurons in the integrative properties of the neostriatum.

Publication types

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

MeSH terms

  • Animals
  • Bicuculline / pharmacology
  • Cell Count
  • Cerebral Cortex / physiology
  • Corpus Striatum / cytology*
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • GABA Antagonists / pharmacology
  • Green Fluorescent Proteins / genetics
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials / drug effects
  • Interneurons / classification*
  • Interneurons / physiology*
  • Lysine / analogs & derivatives
  • Lysine / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nerve Growth Factor / metabolism
  • Neural Pathways / physiology
  • Neuropeptide Y / metabolism*
  • Nitric Oxide Synthase / metabolism
  • Patch-Clamp Techniques
  • Quinoxalines / pharmacology
  • Somatostatin / metabolism

Substances

  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • Neuropeptide Y
  • Quinoxalines
  • Green Fluorescent Proteins
  • Somatostatin
  • FG 9041
  • Nerve Growth Factor
  • Nitric Oxide Synthase
  • biocytin
  • Lysine
  • Bicuculline