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Synaptic Inputs to Trigeminal Primary Afferent Neurons Cause Firing and Modulate Intrinsic Oscillatory Activity

¹Centre de Recherche en Sciences Neurologiques and ²Faculté de Médecine Dentaire, Université de Montréal, Montreal, Quebec H3C 3J7; and ³Faculty of Dentistry, McGill University, Montreal, Quebec H3A 2B2, Canada

Submitted 19 March 2004; accepted in final form 31 May 2004

In this paper, we investigated the influence of synapses on the cell bodies of trigeminal muscle spindle afferents that lie in the trigeminal mesencephalic nucleus (NVmes), using intracellular recordings in brain stem slices of young rats. Three types of synaptic responses could be evoked by electrical stimulation of the adjacent supratrigeminal, motor, and main sensory nuclei and the intertrigeminal area: monophasic depolarizing postsynaptic potentials (PSPs), biphasic PSPs, and all or none action potentials without underlying excitatory PSPs (EPSPs). Many PSPs and spikes were abolished by bath-application of 6,7-dinitroquinoxaline (DNQX) alone or combined with D,L-2-amino-5-phosphonovaleric acid (APV), suggesting that they are mediated by non–N-methyl-D-aspartate (NMDA) and NMDA glutamatergic receptors, while some action potentials were sensitive to bicuculline, indicating involvement of GABA_A receptors. A number of cells showed spontaneous membrane potential oscillations, and stimulation of synaptic inputs increased the amplitude of the oscillations for several cycles, which often triggered repetitive firing. Furthermore, the oscillatory rhythm was reset by the stimulation. Our results show that synaptic inputs to muscle primary afferent neurons in NVmes from neighboring areas are mainly excitatory and that they cause firing. In addition, the inputs synchronize intrinsic oscillations, which may lead to sustained, synchronous firing in a subpopulation of afferents. This may be of importance during rapid biting and during the mastication of very hard or tough foods.

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