Development of resurgent and persistent sodium currents in mesencephalic trigeminal neurons

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Mesencephalic trigeminal (Mes V) neurons relay sensory input from masticatory muscle spindles and periodontal mechanoreceptors and are essential components of oral–motor circuitry (Dessem & Taylor, 1989; Jerge, 1963). The information Mes V neurons receive is transferred to masticatory motoneurons, the thalamus, and various brainstem nuclei (Alvarado‐Mallart, Batini, Buisseret‐Delmas, & Corvisier, 1975; Appenteng, O'Donovan, Somjen, Stephens, & Taylor, 1978; Luo & Dessem, 1995). In the absence of synaptic interactions, Mes V neurons older than postnatal day (P) 7 induce subthreshold oscillations and burst discharges with high‐frequency firing after membrane depolarization and may be capable of rhythmic burst generation because of their unique properties in the trigeminal system (Pedroarena, Pose, Yamuy, Chase, & Morales, 1999; Wu, Hsiao, & Chandler, 2001). Mes V neurons are important for production of appropriate jaw movements for setting the oral–motor rhythm during mastication or sucking (Miles, 1979; Morimoto, Inoue, Masuda, & Nagashima, 1989). These neurons are active during jaw movement, and local stimulation of nearby interneurons in the supratrigeminal area, intertrigeminal area, motor trigeminal nucleus, or the dorsal and medial part of the principal trigeminal sensory nucleus produces synaptic potentials, subthreshold oscillations, and spike activity (Verdier, Lund, & Kolta, 2004). Because Mes V neurons reside within the brainstem, they may function as interneurons (Kolta, Lund, Westberg, & Clavelou, 1995), which has important implications for how they function as generators in oral–motor activities, including physiological movement and pathological disorders.
In addition to producing large, inward currents that underlie fast action potentials, tetrodotoxin (TTX)‐sensitive sodium channels conduct persistent sodium currents (INaP), which may play a major role in regulating repetitive firing (Cepeda, Chandler, Shumate, & Levine, 1995; Crill, 1996; Enomoto, Han, Hsiao, Wu, & Chandler, 2006; French, Sah, Buckett, & Gage, 1990; Taylor, 1993). Subsequent studies of sodium currents in various neurons have also identified resurgent sodium currents (INaR), which may contribute to the propensity of Purkinje or Mes V neurons to fire at high frequency (Enomoto et al., 2006; Raman & Bean, 1997; Raman, Sprunger, Meisler, & Bean, 1997). Single‐channel studies showed that the same TTX‐sensitive sodium channels that also produce fast‐inactivating current carry INaR and express the isoform Nav1.6 (Burgess et al., 1995; Raman & Bean, 1997).
The bursting behavior of Mes V neurons depends on TTX‐sensitive sodium channels (Pedroarena et al., 1999; Wu et al., 2005, 2001). Our previous study showed that INaR and INaP play important roles in driving and maintaining high‐frequency firing during a burst (Enomoto et al., 2006). This burst activity in Mes V neurons emerges after P7 during development in rats. Based on these findings, we investigated the developmental changes in INaR and INaP in rats that may contribute to the burst discharges of Mes V neurons and the increase in occurrence with age. We found a significant increase in current densities in older (>P7) neurons.
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