Specific brainstem neurons switch each other into pacemaker mode to drive movement by activating NMDA receptors

W.-C. Li, A Roberts, SR Soffe

Research output: Contribution to journalArticle (Academic Journal)peer-review

45 Citations (Scopus)

Abstract

Rhythmic activity is central to brain function. In the vertebrate CNS, the neuronal circuits for breathing and locomotion involve inhibition and also neurons acting as pacemakers, but identifying the neurons responsible has proven difficult. By studying simple hatchling Xenopus laevis tadpoles, we have already identified a population of electrically coupled hindbrain neurons (dINs) that drive swimming. During rhythm generation, dINs release glutamate to excite each other and activate NMDA receptors (NMDARs). The resulting depolarization enables a network mechanism for swimming rhythm generation that depends on reciprocal inhibition between antagonistic right and left sides. Surprisingly, a surgically isolated hemi-CNS without inhibition can still generate swimming-like rhythms. We have now discovered that activation ofNMDARstransforms dINs, which normally fire singly to current injection, into pacemakers firing within the normal swimming frequency range (10 –25 Hz). When dIN firing is blocked pharmacologically, this NMDAR activation produces 10 Hz membrane potential oscillations that persist when electrical coupling is blocked but not when the voltage-dependent gating of NMDARs byMg2is removed. The NMDA-induced oscillations and pacemaker firing at swimming frequency are unique to the dIN population and do not occur in other spinal neurons. We conclude that NMDAR-mediated self-resetting switches critical neurons that drive swimming into pacemaker mode only during locomotion where it provides an additional, parallel mechanism for rhythm generation. This allows rhythm generation in a half-CNS and raises the possibility that such concealed pacemaker properties may be present underlying rhythm generation in other vertebrate brain networks.
Translated title of the contributionSpecific brainstem neurons switch each other into pacemaker mode to drive movement by activating NMDARs
Original languageEnglish
Pages (from-to)16609 - 16620
JournalJournal of Neuroscience
Volume30
Issue number49
DOIs
Publication statusPublished - Dec 2010

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