Bimodal modulation of short-term motor memory via dynamic sodium pumps in a vertebrate spinal cord

Lamia Hachoumi, Rebecca Rensner, Claire Richmond, Laurence Picton, HongYan Zhang, Keith T. Sillar*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

6 Citations (Scopus)

Abstract

Dynamic neuronal Na+/K+ pumps normally only respond to intense action potential firing owing to their low affinity for intracellular Na+. Recruitment of these Na+ pumps produces a post-activity ultraslow afterhyperpolarization (usAHP) up to ∼10 mV in amplitude and ∼60 s in duration, which influences neuronal properties and future network output. In spinal motor networks, the usAHP underlies short-term motor memory (STMM), reducing the intensity and duration of locomotor network output in a manner dependent on the interval between locomotor bouts. In contrast to tonically active Na+ pumps that help set and maintain the resting membrane potential, dynamic Na+ pumps are selectively antagonized by low concentrations of ouabain, which, we show, blocks both the usAHP and STMM. We examined whether dynamic Na+ pumps and STMM can be influenced by neuromodulators, focusing on 5-HT and nitric oxide. Bath-applied 5-HT alone had no significant effect on the usAHP or STMM. However, this is due to the simultaneous activation of two distinct 5-HT receptor subtypes (5-HT7 and 5-HT2a) that have opposing facilitatory and suppressive influences, respectively, on these two features of the locomotor system. Nitric oxide modulation exerts a potent inhibitory effect that can completely block the usAHP and erase STMM. Using selective blockers of 5-HT7 and 5-HT2a receptors and a nitric oxide scavenger, PTIO, we further provide evidence that the two modulators constitute an endogenous control system that determines how the spinal network self-regulates the intensity of locomotor output in light of recent past experience.
Original languageEnglish
Pages (from-to)1038-1048.e2
JournalCurrent Biology
Volume32
Issue number5
Early online date31 Jan 2022
DOIs
Publication statusPublished - 14 Mar 2022

Keywords

  • Na+/K+ pump
  • Neuromodulation
  • Afterhyperpolarisation
  • Short-term memory
  • Motor control
  • Xenopus
  • Swimming
  • Locomotion
  • Spinal cord
  • CPG

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