Discharge patterns of trigeminal commissural last-order interneurons during fictive mastication in the rabbit

Abstract

1. The aim of these experiments was to examine the physiological properties and patterns of firing of trigeminal interneurons during fictive mastication in anesthetized and paralyzed rabbits. Antidromic stimulation was used to show that the 82 interneurons projected to the area of the contralateral fifth nerve motor nucleus (NVmot). 2. Straight-line conduction velocities calculated from stereotaxic coordinates of the stimulating and recording electrodes for 63 interneurons were found to range between 3.7 and 16.3 m/s (mean, 9.5 m/s). 3. Histological reconstructions of recording electrode tracks showed that the interneurons observed in this study were located in the lateral brain stem in or just medial to the rostral trigeminal sensory nuclei, including the intertrigeminal (NVint) and supratrigeminal (NVs) areas, the main sensory nucleus of the fifth nerve (NVsnpr), the rostral subdivision of the oral nucleus of the spinal trigeminal tract (NVor tau), and the rostral part of the parvocellular reticular nucleus (NRpc alpha). 4. Forty-six interneurons were shown to have low-threshold (LT) peripheral receptive fields, and 41 of these (88%) were in the oral cavity. Most of the responses were rapidly adapting. 5. Twenty-eight interneurons changed their pattern of firing during cortically induced fictive mastication. The discharge frequency of 20 neurons varied in phase with the fictive masticatory motor output, which was recorded from central ends of cut hypoglossal nerves (XII) and/or from the NVmot. Others were briefly excited and then inhibited (n = 2), only inhibited (n = 4), or tonically excited during fictive mastication (n = 2). Fifteen others were unaffected by this test. 6. It was found that the rhythmically active neurons could be further subdivided into two categories: those receiving short-latency excitatory input from the masticatory area of the cortex (n = 11) and those that did not (n = 9). No obvious differences in peripheral receptive fields for neurons in these categories were found. 7. We suggest that these phasically active premotor neurons are part of the circuitry generating the rhythmic masticatory pattern, specifically those that directly control the bursts of firing of the trigeminal motoneurons (burst generators, BGs). Their properties allow them to integrate sensory information and descending commands with the masticatory rhythm that is probably generated in midline brainstem reticular nuclei.