Evidence for functional compartmentalization of trigeminal muscle spindle afferents during fictive mastication in the rabbit

Primary afferent neurons innervating muscle spindles in jaw-closing muscles have cell bodies in the trigeminal mesencephalic nucleus (NVmes) that are electrically coupled and receive synapses. Each stem axon gives rise to a p eripheral branch and a descending central branch. It was previously shown t hat some spikes generated by constant muscle stretch fail to enter the soma during fictive mastication, The present study examines whether the central axon is similarly controlled. These axons were functionally identified in anaesthetized and paralysed rabbits, and tonic afferent firing was elicited by muscle stretch. For the purpose of comparison, responses were recorded extracellularly both from the somatic region and from the central axon in t he lateral brainstem. Two types of fictive masticatory movement patterns we re induced by repetitive stimulation of the masticatory cortex and monitore d from the trigeminal motor nucleus. Field potentials generated by spike-tr iggered averaging of action potentials from the spindle afferents were empl oyed to determine their postsynaptic effects on jaw-closing motoneurons. To nic firing of 32% NVmes units was inhibited during the jaw-opening phase, b ut spike frequency during closing was almost equal to the control rate duri ng both types of fictive mastication. A similar inhibition occurred during opening in 83% of the units recorded along the central branch. However, fir ing frequency in these was significantly increased during closing in 94%, p robably because of the addition of antidromic action potentials generated b y presynaptic depolarization of terminals of the central branch. These addi tional spikes do not reach the soma, but do appear to excite motoneurons. T he data also show that the duration and/or frequency of firing during the b ursts varied from one pattern of fictive mastication to another. We conclud e that the central axons of trigeminal muscle spindle afferents are functio nally decoupled from their stem axons during the jaw-closing phase of masti cation. During this phase, it appears that antidromic impulses in the centr al axons provide one of the inputs from the masticatory central pattern gen erator (CPG) to trigeminal motoneurons.