Rapid adaptation to elevated extracellular potassium in the pyloric circuit of the crab, Cancer borealis

J Neurophysiol. 2020 May 1;123(5):2075-2089. doi: 10.1152/jn.00135.2020. Epub 2020 Apr 22.

Abstract

Elevated potassium concentration ([K+]) is often used to alter excitability in neurons and networks by shifting the potassium equilibrium potential (EK) and, consequently, the resting membrane potential. We studied the effects of increased extracellular [K+] on the well-described pyloric circuit of the crab Cancer borealis. A 2.5-fold increase in extracellular [K+] (2.5×[K+]) depolarized pyloric dilator (PD) neurons and resulted in short-term loss of their normal bursting activity. This period of silence was followed within 5-10 min by the recovery of spiking and/or bursting activity during continued superfusion of 2.5×[K+] saline. In contrast, when PD neurons were pharmacologically isolated from pyloric presynaptic inputs, they exhibited no transient loss of spiking activity in 2.5×[K+], suggesting the presence of an acute inhibitory effect mediated by circuit interactions. Action potential threshold in PD neurons hyperpolarized during an hour-long exposure to 2.5×[K+] concurrent with the recovery of spiking and/or bursting activity. Thus the initial loss of activity appears to be mediated by synaptic interactions within the network, but the secondary adaptation depends on changes in the intrinsic excitability of the pacemaker neurons. The complex sequence of events in the responses of pyloric neurons to elevated [K+] demonstrates that electrophysiological recordings are necessary to determine both the transient and longer term effects of even modest alterations of K+ concentrations on neuronal activity.NEW & NOTEWORTHY Solutions with elevated extracellular potassium are commonly used as a depolarizing stimulus. We studied the effects of high potassium concentration ([K+]) on the pyloric circuit of the crab stomatogastric ganglion. A 2.5-fold increase in extracellular [K+] caused a transient loss of activity that was not due to depolarization block, followed by a rapid increase in excitability and recovery of spiking within minutes. This suggests that changing extracellular potassium can have complex and nonstationary effects on neuronal circuits.

Keywords: F-I curves; central pattern generator; depolarization block; spike threshold; stomatogastric nervous system.

Publication types

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

MeSH terms

  • Animals
  • Brachyura / physiology*
  • Central Pattern Generators / metabolism
  • Central Pattern Generators / physiology*
  • Electrophysiological Phenomena / physiology*
  • Ganglia, Invertebrate / metabolism
  • Ganglia, Invertebrate / physiology*
  • Male
  • Potassium / metabolism*
  • Pylorus / metabolism
  • Pylorus / physiology*

Substances

  • Potassium