Evaluation of mechanisms involved in regulation of intrinsic excitability by extracellular calcium in CA1 pyramidal neurons of rat

J Neurochem. 2025 Jan;169(1):e16209. doi: 10.1111/jnc.16209. Epub 2024 Aug 20.

Abstract

It is well recognized that changes in the extracellular concentration of calcium ions influence the excitability of neurons, yet what mechanism(s) mediate these effects is still a matter of debate. Using patch-clamp recordings from rat hippocampal CA1 pyramidal neurons, we examined the contribution of G-proteins and intracellular calcium-dependent signaling mechanisms to changes in intrinsic excitability evoked by altering the extracellular calcium concentration from physiological (1.2 mM) to a commonly used experimental (2 mM) level. We find that the inhibitory effect on intrinsic excitability of calcium ions is mainly expressed as an increased threshold for action potential firing (with no significant effect on resting membrane potential) that is not blocked by either the G-protein inhibitor GDPβS or the calcium chelator BAPTA. Our results therefore argue that in the concentration range studied, G-protein coupled calcium-sensing receptors, non-selective cation conductances, and intracellular calcium signaling pathways are not involved in mediating the effect of extracellular calcium ions on intrinsic excitability. Analysis of the derivative of the action potential, dV/dt versus membrane potential, indicates a current shift towards more depolarized membrane potentials at the higher calcium concentration. Our results are thus consistent with a mechanism in which extracellular calcium ions act directly on the voltage-gated sodium channels by neutralizing negative charges on the extracellular surface of these channels to modulate the threshold for action potential activation.

Keywords: CaSR; NALCN; calcium; hippocampus; neuronal excitability.

MeSH terms

  • Action Potentials* / drug effects
  • Action Potentials* / physiology
  • Animals
  • CA1 Region, Hippocampal* / drug effects
  • CA1 Region, Hippocampal* / metabolism
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology
  • Calcium* / metabolism
  • Extracellular Space / metabolism
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Patch-Clamp Techniques
  • Pyramidal Cells* / drug effects
  • Pyramidal Cells* / metabolism
  • Pyramidal Cells* / physiology
  • Rats
  • Rats, Wistar

Substances

  • Calcium