Spontaneous Discharge and Peripherally Evoked Orofacial Responses of Trigemino–Thalamic Tract Neurons during Wakefulness and Sleep

Abstract

In the present study, ongoing and evoked activity of antidromically identified trigemino-thalamic tract (TGT) neurons was examined over the sleep-wake cycle in cats. There was no difference in the mean spike discharge rate of TGT neurons when quiet sleep (QS) and active sleep (AS) were compared with wakefulness (W). However, tooth pulp-evoked responses of TGT neurons were decreased during AS when compared to W. Conversely, the responses of TGT neurons to air puff activation of facial hair mechanoreceptors reciprocally increased during AS when compared to W. The present data demonstrate that ascending sensory information emanating from distinct orofacial areas is differentially modified during the behavioral state of AS. Specifically, the results obtained suggest that during AS, sensory information arising from hair mechanoreceptors is enhanced, whereas information arising from tooth pulp afferents is suppressed. These data may provide functional evidence for an AS-related gate control mechanism of sensory outflow to higher brain centers. Key words: behavioral state; brainstem; hair mechanoreceptor; main sensory nucleus; nucleus oralis; sensory; sleep; tooth pulp; trigeminothalamicThe trigemino-thalamic tract (TGT) is a major somatosensory pathway that conveys sensory information from orofacial regions rostrally to the thalamus and on to the cerebral cortex. Both electrophysiological (Sessle and Greenwood, 1976;Sessle and Hu, 1981;Azerad et al., 1982;Sunada et al., 1990;Ro and Capra, 1994) and anatomical labeling (Mizuno, 1970;Woda et al., 1977;Burton and Craig, 1979;Matsushita et al., 1982;Shigenaga et al., 1986;Matthews et al., 1987Matthews et al., , 1989) studies performed in acute anesthetized cats have demonstrated that the rostral trigeminal sensory nuclear complex (TSNC) comprising, respectively, the nucleus oralis and the main sensory nucleus, contains a high density of TGT neurons. Recently, we have shown that the tooth pulp-evoked activity of rostral TSNC neurons is suppressed specifically during the behavioral state of active (AS) or REM sleep . However, the axonal projection of the recorded cells was not determined.Given the high density of TGT neurons located in the rostral TSNC in concert with our recent findings of AS-related suppression of these neurons, we hypothesize that synaptic transmission via the TGT is suppressed during the behavioral state of AS. To test this hypothesis, the present study was performed to identify TGT neurons and measure their ongoing and peripherally evoked activity recorded during sleep and wakefulness in chronically instrumented behaving cats. The results obtained via stimuli applied to tooth pulp afferents versus facial hair mechanoreceptors suggest that the source of the peripheral input used to activate the recorded neurons is critical in determining the active sleep-related changes that occur in synaptic transmission through the TGT.

Disparate cholinergic currents in rat principal trigeminal sensory nucleus neurons mediated by M1 and M2 receptors: a possible mechanism for selective gating of afferent sensory neurotransmission

“…, 1994; Marrosu et al. , 1995; Vazquez & Baghdoyan, 2001), and the excitability of PSTN neurons changes during active sleep relative to wakefulness (Cairns et al. , 1995, 1996a,b) in a modality‐specific manner (Cairns et al.…”

“…Moreover, although the overall firing rates for the spontaneously active PSTN cell subpopulation, as a whole, do not seem to vary systematically between sleep and wakefulness (Cairns et al. , 1996b), discharge patterns of individual trigemino‐thalamic tract cells are modulated during quiet sleep or active sleep and its substages (Cairns et al. , 1996b; Kristensen et al.…”

“…Chronic recording studies found attenuated tooth pulp‐evoked responses of neurons in the principal sensory trigeminal nucleus (PSTN) during the state of active sleep relative to wakefulness (Cairns et al. , 1995, 1996a,b).…”

Sleep, pain, fibromyalgia, and chronic fatigue syndrome

“…Sensory gating in the trigeminal nucleus or in spinal cord neurons that give rise to ascending somatosensory tracts has been addressed in a few animal studies. Decreased sensory-evoked discharge rates in the trigeminal complex have been recorded during REM sleep compared to wakefulness and NREM sleep (Satoh et al, 1980a, b), but responses to air puff stimuli applied to the face were actually increased during REM sleep in the cat (Cairns et al, 1996). Hernandez-Peon and colleagues (1965) conducted one of the first physiological recordings of evoked potentials in the trigeminal nucleus during sleep in cats and found that responses to stimulation of the skin of the face were stable during quiet wakefulness and reduced during behavioral alertness and REM sleep.…”

Both oral and caudal parts of the spinal trigeminal nucleus project to the somatosensory thalamus in the rat

“…To address this issue, we investigated whether Sp5O neurons project to the main relays of ascending trigeminal somatosensory information to the primary somatic sensory cortex (Price & Dubner, 1977): the medial division of the ventroposterior thalamic nucleus (VPM) and the posterior thalamic nuclear group (Po) (Price, 1995). Indeed, while antidromic potentials have consistently been recorded in cat Sp5O following thalamic stimulation (Azerad et al ., 1982; Cairns et al ., 1996), one single report has been made in rat (Tabata et al ., 2001). Furthermore, results of anatomical studies using retrograde tracers appear controversial in rats (Fukushima & Kerr, 1979; Erzurumlu et al ., 1980; Bruce et al ., 1987; Mantle‐St.John & Tracey, 1987; Patrick & Robinson, 1987; Kemplay & Webster, 1989; Luo & Dessem, 1995), and a single work using the anterograde tracer Phaseolus vulgaris has suggested the existence of a trigeminothalamic pathway emanating from the Sp5O (De Chazeron et al ., 2004).…”