Intracellular response properties of neurons in the spinal trigeminal nucleus to peripheral and cortical stimulation in the cat

Sunada, Takeomi; Kurasawa, Ikufumi; Hirose, Yasuyuki; Nakamura, Yoshio

doi:10.1016/0006-8993(90)91415-d

Cited by 14 publications

(5 citation statements)

References 27 publications

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“…2 A) is similar to antidromic latencies reported in acute studies (Dubner and Sessle, 1971;Sessle and Greenwood, 1976;Dostrovsky and Hellon, 1978;Hu et al, 1981;Sessle and Hu, 1981;Hyashi et al, 1984;Amano et al, 1986;Sunada et al, 1990;Ro and Capra, 1994).…”

Section: Identification Of Tgt Neurons In the Awake Catsupporting

confidence: 70%

“…This was accomplished by combining extracellular recording methodologies with classical antidromic techniques to identify TGT neurons in unanesthetized cats. The basic physiological characteristics of these neurons, i.e., antidromic latency and conduction velocity, and their anatomical location substantiate results obtained for TGT neurons in acute anesthetized cats (Mizuno, 1970;Dubner and Sessle, 1971;Sessle and Greenwood, 1976;Dostrovsky and Hellon, 1978;Burton and Craig, 1979;Hu et al, 1981;Sessle and Hu, 1981;Matsushita et al, 1982;Hyashi et al, 1984;Matthews et al, 1987;Sunada et al, 1990;Ro and Capra, 1994).…”

Section: Characteristics Of Tgt Neurons In the Awake Catmentioning

confidence: 60%

“…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 .…”

mentioning

confidence: 99%

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

et al. 1996

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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.

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Section: Identification Of Tgt Neurons In the Awake Catsupporting

confidence: 70%

Section: Characteristics Of Tgt Neurons In the Awake Catmentioning

confidence: 60%

mentioning

confidence: 99%

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

et al. 1996

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“…Thus, the above-described local-circuit neurons or premotoneurons are considered to be cells of origin of P-endings and to modulate activity of the second-order neurons presynaptically. Axodendritic synapses from Pendings may be responsible for peripherally induced postsynaptic inhibition, described by Ishimine et al (1980) and Sunada et al (1990) in the trigeminal sensory nucleus. These inhibitory processes may relate to sharpening spatial information and to suppression of a long-lasting spike generation in the second-order neurons.…”

Section: Synaptic Organization Associated With Labeled Boutonsmentioning

confidence: 99%

Morphology and synaptic connections of slowly adapting periodontal afferent terminals in the trigeminal subnuclei principalis and oralis of the cat

Bae

Nakagawa

Yoshida

et al. 1994

J of Comparative Neurology

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Previous studies suggest that sensory information from primary afferent fibers is processed in a distinct manner in the individual subnuclei of trigeminal sensory nuclear complex. The present study has addressed this issue by using intra-axonal labeling with horseradish peroxidase to examine the ultrastructure and synaptic organization of axon terminals from slowly adapting (SA) periodontal afferents in the ventral subdivision (Vpv) of principalis and the rostro-dorsomedial part (Vo.r) of oralis. Our observations are based on complete or near-complete reconstructions of 139 synaptic boutons in Vpv and 105 in Vo.r. All the labeled boutons contained clear, spherical, synaptic vesicles and were presynaptic to unlabeled dendrites, and they were frequently postsynaptic to unlabeled axon terminals containing pleomorphic synaptic vesicles (P-endings). The P-endings frequently formed axodendritic synapses on dendrites which received axodendritic synapses from labeled boutons (synaptic triads). On the basis of the number of contacts, synaptic arrangements associated with the labeled boutons could be subgrouped into simple (one or two contacts), intermediate (three or four contacts), and complex (five or more contacts) types. The labeled boutons varied from round to elongated forms with smooth to more irregular or scalloped contours. The boutons with scalloped contour were much more frequent in the complex type. The boutons of the intermediate type were significantly smaller than the complex type and larger than the simple type. The SA periodontal afferent terminals participated in each type of synaptic arrangements in Vpv, but were mostly of the simple type in Vo.r. The size of labeled boutons was significantly larger in Vpv than in Vo.r. The total number of axodendritic and axoaxonic contacts per labeled bouton was significantly higher in Vpv than in Vo.r. Another difference was the more frequent occurrence of synaptic triads in Vpv than in Vo.r. These observations provide evidence that sensory information from primary afferent fibers is processed in a different manner in the two subnuclei.

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“…Neurons, including trigeminal sensory neurons, communicate through APs generated in response to a stimulus ( Sunada et al, 1990 ; Chudler et al, 1991 ; Coste et al, 2008 ). The timing and frequency of spikes are essential for encoding information ( Eggermont, 1998 ; Masuda and Aihara, 2007 ) and, therefore, should be correctly modulated in response to changes in the extracellular milieu.…”

Section: Discussionmentioning

confidence: 99%

Overexpressed NaV1.7 Channels Confer Hyperexcitability to in vitro Trigeminal Sensory Neurons of CaV2.1 Mutant Hemiplegic Migraine Mice

Mehboob¹,

Marchenkova²,

Maagdenberg³

et al. 2021

Front. Cell. Neurosci.

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Trigeminal sensory neurons of transgenic knock-in (KI) mice expressing the R192Q missense mutation in the α1A subunit of neuronal voltage-gated CaV2.1 Ca2+ channels, which leads to familial hemiplegic migraine type 1 (FHM1) in patients, exhibit a hyperexcitability phenotype. Here, we show that the expression of NaV1.7 channels, linked to pain states, is upregulated in KI primary cultures of trigeminal ganglia (TG), as shown by increased expression of its α1 subunit. In the majority of TG neurons, NaV1.7 channels are co-expressed with ATP-gated P2X3 receptors (P2X3R), which are important nociceptive sensors. Reversing the trigeminal phenotype with selective CaV2.1 channel inhibitor ω-agatoxin IVA inhibited NaV1.7 overexpression. Functionally, KI neurons revealed a TTX-sensitive inward current of larger amplitude that was partially inhibited by selective NaV1.7 blocker Tp1a. Under current-clamp condition, Tp1a raised the spike threshold of both wild-type (WT) and KI neurons with decreased firing rate in KI cells. NaV1.7 activator OD1 accelerated firing in WT and KI neurons, a phenomenon blocked by Tp1a. Enhanced expression and function of NaV1.7 channels in KI TG neurons resulted in higher excitability and facilitated nociceptive signaling. Co-expression of NaV1.7 channels and P2X3Rs in TGs may explain how hypersensitivity to local stimuli can be relevant to migraine.

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Intracellular response properties of neurons in the spinal trigeminal nucleus to peripheral and cortical stimulation in the cat

Cited by 14 publications

References 27 publications

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

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

Morphology and synaptic connections of slowly adapting periodontal afferent terminals in the trigeminal subnuclei principalis and oralis of the cat

Overexpressed NaV1.7 Channels Confer Hyperexcitability to in vitro Trigeminal Sensory Neurons of CaV2.1 Mutant Hemiplegic Migraine Mice

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