Histamine H3 receptor activation increases the firing of striatal medium spiny neurons in slices from infantile rats

Can J Physiol Pharmacol. 2025 Apr 1;103(4):134-145. doi: 10.1139/cjpp-2024-0240. Epub 2025 Feb 13.

Abstract

Striatal medium spiny neurons (MSN) form two subpopulations (MSN-D1 and MSN-D2) according to the expression of dopamine D1 or D2 receptors and their target regions. The activation of postsynaptic histamine H1 and H2 receptors increases MSN-D1 and MSN-D2 excitability. Since MSN also express H3 receptors (H3Rs), in this work we explored the effect of their activation on MSN firing. Electrophysiological recordings (whole-cell patch-clamp, current-clamp mode) were conducted on forebrain slices from infantile rats (12-16 postnatal days). In both MSN-D1 and MSN-D2 perfusion with the H3R agonist immepip (1 µmol/L) increased neuronal firing evoked by current injection, an effect reproduced by R-α-methylhistamine (1 µmol/L) and prevented by the antagonist clobenpropit (10 µmol/L). Blockade of N- or P/Q-type voltage-activated calcium channels by ω-conotoxin-GVIA (1 µmol/L) or ω-agatoxin-TK (400 nmol/L) increased MSN firing but did not preclude the immepip effect. The potassium channel blockers 4-aminopyridine (1 mmol/L) and tetraethylammonium (300 µmol/L) increased neuronal firing and prevented the immepip action. Likewise, the KV7 channel blocker XE-991 (10 µmol/L) and the muscarinic receptor agonist carbachol (10 µmol/L) increased MSN firing frequency and occluded the immepip effect. These data indicate that the activation of postsynaptic H3Rs facilitates MSN-D1 and MSN-D2 firing by inhibiting KV7 potassium channels.

Keywords: H3 receptors; histamine; medium spiny neurons; potassium channels; striatum.

MeSH terms

  • Action Potentials* / drug effects
  • Animals
  • Animals, Newborn
  • Corpus Striatum* / cytology
  • Corpus Striatum* / drug effects
  • Corpus Striatum* / metabolism
  • Corpus Striatum* / physiology
  • Histamine Agonists / pharmacology
  • Male
  • Medium Spiny Neurons
  • Neurons* / drug effects
  • Neurons* / metabolism
  • Neurons* / physiology
  • Rats
  • Rats, Wistar
  • Receptors, Histamine H3* / metabolism

Substances

  • Receptors, Histamine H3
  • Histamine Agonists