Intrinsic burst-firing in lamina I spinoparabrachial neurons during adolescence

Neurosci Lett. 2021 Apr 17;750:135794. doi: 10.1016/j.neulet.2021.135794. Epub 2021 Mar 2.

Abstract

A subset of glutamatergic interneurons in the neonatal spinal superficial dorsal horn (SDH) exhibits intrinsic burst-firing (i.e. 'pacemaker' activity), which is tightly regulated by persistent, voltage-gated Na+ channels and classic inward-rectifying K+ (Kir2) channels and downregulated over the course of postnatal development. Ascending lamina I projection neurons targeting the parabrachial nucleus (PB) or periaqueductal gray (PAG) can also display pacemaker activity during early life. However, the degree to which the ionic mechanisms driving pacemaker activity are conserved across different cell types in the spinal dorsal horn, as well as whether the intrinsic bursting is restricted to newborn projection neurons, remains to be elucidated. Using in vitro patch clamp recordings from identified lamina I spinoparabrachial neurons in rat spinal cord slices, here we demonstrate that adolescent projection neurons retain their ability to generate pacemaker activity. In contrast to previous findings in lamina I interneurons, pacemaker projection neurons possessed higher membrane capacitance, lower membrane resistance, and a greater Kir-mediated conductance compared to adjacent spinoparabrachial neurons that lacked intrinsic burst-firing. Nonetheless, as previously seen in interneurons, the bath application of riluzole to block persistent Na+ channels significantly dampened pacemaker activity in projection neurons. Collectively, these results suggest that intrinsic burst-firing in the developing dorsal horn can be generated by multiple combinations of ionic conductances, and highlight the need for further investigation into the mechanisms governing pacemaker activity within the major output neurons of the SDH network.

Keywords: Burst-firing; Dorsal horn; Patch clamp; Projection neuron; Spinal cord.

Publication types

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

MeSH terms

  • Action Potentials*
  • Animals
  • Biological Clocks
  • Female
  • Male
  • Neurons / metabolism
  • Neurons / physiology*
  • Parabrachial Nucleus / cytology
  • Parabrachial Nucleus / growth & development
  • Parabrachial Nucleus / physiology*
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Sodium Channels / metabolism
  • Spinal Cord Dorsal Horn / cytology
  • Spinal Cord Dorsal Horn / growth & development
  • Spinal Cord Dorsal Horn / physiology*

Substances

  • Potassium Channels, Inwardly Rectifying
  • Sodium Channels