C-type natriuretic peptide modulates bidirectional plasticity in hippocampal area CA1 in vitro

Neuroscience. 2010 Aug 11;169(1):8-22. doi: 10.1016/j.neuroscience.2010.04.064. Epub 2010 May 8.

Abstract

C-type natriuretic peptide (CNP) and the natriuretic peptide receptor B (NPR-B) are expressed throughout the hippocampus. We tested whether CNP affected long-term potentiation (LTP) or long-term depression (LTD) in area CA1. Field potentials (FP) were simultaneously recorded in stratum pyramidale (SP) and stratum radiatum (SR) of area CA1 in rat hippocampal slices. To induce LTD and LTP stimulation was applied to SR in area CA1 at 1 and 5 Hz and 30-100 Hz, respectively. CNP (100 nM) increased LTD magnitude while LTP induction was impeded. Thus, in the presence of CNP the threshold for LTP induction was shifted to higher stimulus frequencies, a modulation that showed layer-specific differences in area CA1. Effects of CNP were prevented by the NPR-B antagonist HS-142-1. In the presence of the GABA(A) receptor blocker bicuculline (BMI, 5 microM), CNP-mediated effects were attenuated in SP and SR. Intracellular recordings under this condition revealed that CNP significantly reduced number of action potentials generated during depolarizing current steps. The input resistance of CA1 cells and amplitude of isolated excitatory postsynaptic potential (EPSPs) were significantly increased by CNP whereas these changes were not observed in the absence of BMI. 100 Hz stimulation induced stable potentiation of the EPSP amplitude in CA1 pyramidal cells while this effect was strongly attenuated by CNP. This effect was prevented by BMI. Immunohistochemistry indicated that the peptide binds to receptors expressed on pyramidal cells and GAD(65/67)-immunopositive interneurons. 20 Hz stimulation, applied for 30 s, induced LTP in SR and SP. CNP attenuated LTP in SP and reversed LTP into LTD in SR. These effects were mimicked by low-dose dl-2-amino-5-phosphonopentanoic acid (dl-APV) (10 microM) suggesting partial N-methyl d-aspartate (NMDA) receptor dependency of CNP-mediated effects. Together, our data suggest that CNP is involved in the regulation of bidirectional plasticity in area CA1 potentially by modulating GABA(A)-mediated inhibition and NMDA receptors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / analogs & derivatives
  • 2-Amino-5-phosphonovalerate / pharmacology
  • Action Potentials / drug effects
  • Animals
  • Bicuculline / pharmacology
  • CA1 Region, Hippocampal / drug effects
  • CA1 Region, Hippocampal / physiology*
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Female
  • GABA Antagonists / pharmacology
  • In Vitro Techniques
  • Interneurons / drug effects
  • Interneurons / physiology
  • Long-Term Potentiation / drug effects
  • Long-Term Potentiation / physiology*
  • Long-Term Synaptic Depression / drug effects
  • Long-Term Synaptic Depression / physiology*
  • Natriuretic Peptide, C-Type / antagonists & inhibitors
  • Natriuretic Peptide, C-Type / pharmacology
  • Natriuretic Peptide, C-Type / physiology*
  • Polysaccharides / pharmacology
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / physiology
  • Rats
  • Rats, Wistar
  • Receptors, Atrial Natriuretic Factor / agonists
  • Receptors, Atrial Natriuretic Factor / physiology
  • Receptors, GABA-A / physiology*

Substances

  • Excitatory Amino Acid Antagonists
  • GABA Antagonists
  • HS 142-1
  • Polysaccharides
  • Receptors, GABA-A
  • 2-amino-5-phosphono-3-pentenoic acid
  • Natriuretic Peptide, C-Type
  • 2-Amino-5-phosphonovalerate
  • Receptors, Atrial Natriuretic Factor
  • atrial natriuretic factor receptor B
  • Bicuculline