Metabotropic glutamate receptor activity induces a novel oscillatory pattern in neonatal rat hypoglossal motoneurones

Tongue muscles innervated by the hypoglossal nerves play a crucial role to ensure airway patency and milk suckling in the neonate. Using a slice preparation of the neonatal rat brain, we investigated the electrophysiological characteristics of hypoglossal motoneurones in the attempt to identify certain properties potentially capable of synchronizing motor commands to the tongue. Bath-applied DHPG, a selective agonist of group I metabotropic glutamate receptors (mGluRs), generated persistent, regular electrical oscillations (4-8 Hz) recorded from patch-clamped motoneurones. Under voltage clamp, oscillations were biphasic events, comprising large outward slow currents alternated with fast, repeated inward currents. Electrical oscillations had amplitude and period insensitive to cell membrane potential, and required intact glutamatergic transmission via AMPA receptors. Oscillations were mediated by subtype 1 receptors of group I mGluRs (mGluR1s), and were routinely observed during pharmacological block of glycinergic and GABAergic inhibition, although they could also be recorded in standard saline. Simultaneous recordings from pairs of motoneurones within the same hypoglossal nucleus demonstrated that oscillations were due to their strong electrical coupling and were blocked by the gap junction blocker carbenoxolone. Pacing of slow oscillations apparently depended on the operation of K(ATP) channels in view of the block by tolbutamide or glibenclamide. Under current clamp, oscillations generated more regular spike firing of motoneurones and facilitated glutamatergic excitatory inputs. These data suggest that neonatal motoneurones of the nucleus hypoglossus possess a formerly undisclosed ability to express synchronous electrical oscillations, unveiled by activation of mGluR1s.