Effect of the stimulation of sensory inputs on the firing of neurons of the trigeminal main sensory nucleus in the rat

Abstract

Mastication can be triggered by repetitive stimulation of the cortex or of sensory inputs, but is patterned by a brain stem central pattern generator (CPG). This CPG may include the dorsal part of the principal trigeminal sensory nucleus (NVsnpr), where neurons burst repetitively when the extracellular concentration of Ca(2+) ([Ca(2+)](e)) drops. We examined the effects of repetitive stimulation of sensory afferents of the trigeminal tract on activity of NVsnpr neurons recorded extracellularly in vitro under physiologic [Ca(2+)](e) (1.6 mM). Spontaneously active cells had either a tonic (n = 145) or a bursting (n = 46) firing pattern. Afferent stimulation altered burst duration and/or burst frequency in bursting cells and firing frequency in most tonic cells. In 28% of the latter, the firing pattern switched to rhythmic bursting. This effect could be mimicked by local application of N-methyl-d-aspartate and blocked by APV but not DNQX. Detailed analysis showed that rhythm indices (RIs) of 35 tonic neurons that were negative (nonrhythmic) before stimulation became significantly rhythmic (RI > or = 0.01) after stimulation. Mean and median bursting frequency of these units were 8.32 +/- 0.72 (SE) Hz and 6.25 Hz (range, 2.5-17.5 Hz). In seven instances, two units were recorded simultaneously, and cross-correlation analysis showed that firing of six pairs was rhythmic and synchronized after stimulation. Optimal stimulation parameters for eliciting rhythmic bursting consisted in 500-ms trains of pulses delivered at 40-60 Hz. Together, our results show that repetitive stimulation of sensory afferents in vitro can elicit masticatory-like rhythmic bursting in NVsnpr neurons at physiological [Ca(2+)](e).