In trigeminal neurons, the spike rate, modulated by input parameters, may serve as
a code for sensory information. We investigated intrinsic response properties that
affect rate coding in neurons of nucleus principalis trigemini (young gerbils). Using
the whole-cell recording technique and neurobiotin staining in slices, we found bursting
behaviour in approximately 50% of the neurons. These neurons fired spike bursts, spontaneously,
as well as at the onset of depolarizing, and offset of hyperpolarizing, current pulses.
The spike rate within an initial burst was independent of stimulus strength, in contrast
to single spike firing that occurred later in the response to current pulse injection.
The spikes within a burst were superimposed on slow depolarizing humps. Under favourable
conditions, these led to "plateau potentials", that lasted for hundreds of milliseconds
at membrane potentials near approximately -20 mV. Occasionally, plateau potentials
were spontaneous or evoked under control conditions: usually, they were evoked by
current pulse injection during blockade of Ca2+ influx with Co2+ or Cd2+ in Ca(2+)-free
extracellular media, or during blockade of K+ currents with tetraethylammonium. The
plateau potentials recorded during internal Cs+ (132.5 mM) substitution of K+ had
more positive amplitudes (near +20 mV). Despite relatively stable depolarization levels,
the plateau potentials decreased in duration and decayed in amplitude during application
of tetrodotoxin (0.6-1.8 nM). Higher tetrodotoxin concentrations (5-60 nM) eliminated
the plateau potentials despite well-maintained, fast action potentials. A reduction
of external [Na+] reduced the amplitudes of the spikes and plateau potentials. A hyperpolarization
of long duration (> 3 s) followed a plateau potential, or a depolarizing response
that was subthreshold for plateau generation. Tetrodotoxin application blocked this
after-effect. We suggest that a persistent Na+ influx is a major contributor to the
bursts and plateau potentials and that it mediates the hyperpolarization. Depending
on Ca2+ influx, K+ conductances may regulate the amplitudes of these long-lasting
depolarizations. A Ca2+ conductance, blockable by Ni2+, may support burst initiation
in these neurons. In very young animals (P2-P9), we found only non-bursting neurons.
Both bursting and non-bursting neurons with elongated dendritic fields showed inward
rectification on hyperpolarization. The bursts in nucleus principalis trigemini neurons
emphasize the onsets of stimulus transients, at the expense of using firing rate as
a sensory code. Our studies describe neurons with a surprising ability to distort
sensory signals, transforming depolarizing inputs into bursts of spikes by virtue
of a Na(+)-conductance activation. The principal trigeminal nucleus also contains
neurons with tonic firing ability, compatible with simple rate coding.