Intrinsic response properties of bursting neurons in the nucleus principalis trigemini of the gerbil.
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.
Sandler
V M
VM
Department of Surgery, Faculty of Medicine, University of British Columbia, Vancouver, Canada.
Puil
E
E
Schwarz
D W
DW
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D002118:Calcium / Q000378:metabolism; D002462:Cell Membrane / Q000502:physiology; D002794:Choline / Q000494:pharmacology; D003712:Dendrites / Q000648:ultrastructure; D004553:Electric Conductivity; D004594:Electrophysiology; D005849:Gerbillinae; D009474:Neurons / Q000187:drug effects / Q000502:physiology*; D011188:Potassium / Q000502:physiology; D012964:Sodium / Q000502:physiology; D013779:Tetrodotoxin / Q000494:pharmacology; D014278:Trigeminal Nuclei / Q000166:cytology / Q000187:drug effects / Q000502:physiology*
D013779:Tetrodotoxin; D012964:Sodium; D002794:Choline; D011188:Potassium; D002118:Calcium