Summary
Intra-axonal recordings were made from trigeminal primary afferent fibers in the trigeminal spinal nuclei oralis and caudalis of cats. Primary afferent depolarization (PAD) was evoked in these afferents by stimulation of the trigeminal peripheral sensory branches (the frontal, infraorbital and lingual nerves), the cerebral cortex and the trigeminal spinal nucleus caudalis. The properties of the PAD, including the threshold, latency, receptive field (sensory branches effective for PAD induction) and frequency-following capacity, were studied with the following results:
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1.
Stimulation of all the peripheral branches tested as well as the cerebral cortex could evoke PAD in the same single fiber. The latency of the PAD evoked by stimulation of the nerve in which the fiber being recorded from was included was generally shorter than that evoked by other branches. The PAD evoked by peripheral nerve stimulation was assumed to be disynaptic in some cases.
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2.
The peripherally evoked PAD was chiefly attributable to low threshold afferents in the stimulated sensory branches of the trigeminal nerve.
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3.
The peripherally evoked PAD could follow stimulation at up to 30/sec, though the amplitude was reduced.
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4.
Stimulation of the nucleus caudalis could evoke PAD with disynaptic latency in the majority of the fibers terminating in the same nucleus, whereas it evoked PAD with mainly polysynaptic latency in the fibers terminating in the nucleus oralis.
The results are discussed in relation to the neuronal circuitry responsible for induction of the trigeminal PAD.
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References
Andersen, P., Eccles, J.C., Schmidt, R.F., Yokota, T.: Depolarization of presynaptic fibers in the cuneate nucleus. J. Neurophysiol. 27, 92–106 (1964)
Baldissera, F., Broggi, G., Mancia, M.: Depolarization of trigeminal afferents induced by stimulation of brain-stem and peripheral nerves. Exp. Brain Res. 4, 1–17 (1967)
Darian-Smith, I.: Presynaptic component in the afferent inhibition observed within trigeminal brain-stem nuclei of the cat. J. Neurophysiol. 28, 695–709 (1965)
Darian-Smith, I., Yokota, T.: Cortically evoked depolarization of trigeminal cutaneous afferent fibers in the cat. J. Neurophysiol. 29, 170–184 (1966a)
Darian-Smith, I., Yokota, T.: Corticofugal effects on different neuron types within the cat's brain stem activated by tactile stimulation on the face. J. Neurophysiol. 29, 185–206 (1966b)
Dubner, R., Sessle, B.J.: Presynaptic excitability changes of primary afferent and corticofugal fibers projecting to trigeminal brain stem nuclei. Exp. Neurol. 30, 223–238 (1971)
Eccles, J.C., Kostyuk, P.G., Schmidt, R.F.: Central pathways responsible for depolarization of primary afferent fibers. J. Physiol. (Lond.) 161, 237–257 (1962)
Eccles, J.C., Krnjević, K.: Potential changes recorded inside primary afferent fibers within the spinal cord. J. Physiol. (Lond.) 149, 250–273 (1959)
Gobel, S.: Structural organization in the main sensory trigeminal nucleus. In: Oral-Facial Sensory and Motor Mechanisms (eds. R. Dubner, Y. Kawamura), pp. 183–204. New York: Appleton-Century-Crofts 1971
Gobel, S.: Synaptic organization of the substantia gelatinosa glomeruli in the spinal trigeminal nucleus. J. Neurocytol. 3, 219–243 (1974)
Gobel, S., Dubner, R.: Fine structural studies of the main sensory trigeminal nucleus in the cat and rat. J. comp. Neurol. 137, 459–493 (1969)
Gobel, S., Purvis, M.B.: Anatomical studies of the organization of the spinal V nucleus: the deep bundles and the spinal V tract. Brain Res. 48, 27–44 (1972)
Goldberg, L.J.: Excitatory and inhibitory effects of lingual nerve stimulation on reflexes controlling the activity of masseteric motoneurons. Brain Res. 39, 95–108 (1972)
Goldberg, L.J., Browne, P.A.: Differences in the excitability of two populations of trigeminal primary afferent central terminals. Brain Res. 77, 195–209 (1974)
Hammer, B., Tarnecki, R., Vyklický, L., Wiesendanger, M.: Corticofugal control of presynaptic inhibition in the spinal trigeminal complex of the cat. Brain Res. 2, 216–218 (1966)
Jankowska, E., Roberts, W.J.: Synaptic actions of single interneurones mediating reciprocal Ia inhibition of motoneurones. J. Physiol. (Lond.) 222, 623–642 (1972)
Kerr, F.W.L.: The organization of primary afferents in the subnucleus caudalis of the trigeminal: a light and electron microscopic study of degeneration. Brain Res. 23, 147–165 (1970)
Kidokoro, Y., Kubota, K., Shuto, S., Sumino, R.: Reflex organization of cat masticatory muscles. J. Neurophysiol. 31, 695–708 (1968a).
Kidokoro, Y., Kubota, K., Shuto, S., Sumino, R.: Possible interneurons responsible for reflex inhibition of motoneurons of jaw-closing muscles from the inferior dental nerve. J. Neurophysiol. 31, 709–716 (1968b)
Koketsu, K.: Intracellular potential changes of primary afferent nerve fibers in spinal cords of cats. J. Neurophysiol. 19, 375–392 (1956)
Nakamura, Y., Goldberg, L.J., Clemente, C.D.: Nature of suppression of the masseteric monosynaptic reflex induced by stimulation of the orbital gyrus of the cat. Brain Res. 6, 184–198 (1967)
Nakamura, Y., Murakami, T., Ishimine, S.: Trigeminal PAD as disynaptically evoked by stimulation of the trigeminal sensory branches. Brain Res. 72, 311–314 (1974)
Nakamura, Y., Wu, C.Y.: Presynaptic inhibition of jaw-opening reflex by high-threshold afferents from the masseter muscle of the cat. Brain Res. 23, 193–211 (1970)
Sauerland, E.K., Mizuno, N.: Cortically induced presynaptic inhibition of trigeminal proprioceptive afferents. Brain Res. 13, 556–568 (1969)
Scibetta, C.J., King, R.B.: Hyperpolarizing influence of trigeminal nucleus caudalis on primary afferent preterminals in trigeminal nucleus oralis. J. Neurophysiol. 32, 229–238 (1969)
Shende, M.C., King, R.B.: Excitability changes of trigeminal primary afferent preterminals in brain-stem nuclear complex of squirrel monkey (Saimiri sciureus). J. Neurophysiol. 30, 949–963 (1967)
Stewart, W.A., King, R.B.: Fiber projections from the nucleus caudalis of the spinal trigeminal nucleus. J. comp. Neurol. 121, 271–286 (1963)
Stewart, D.H., Jr., Scibetta, C.J., King, R.B.: Presynaptic inhibition in the trigeminal relay nuclei. J. Neurophysiol. 30, 135–153 (1967)
Van Harreveld, A., Niechaj, A.: A possibly monosynaptic component of the dorsal root potential. Brain Res. 19, 105–116 (1970)
Vyklický, L., Maksimová, E.V., Jirousek, J.: Neurones in the reflex pathway between trigeminal sensory fibers in the cat. Physiol. bohemoslov. 16, 285–296 (1967)
Wall, P.D.: Excitability changes in afferent fiber terminations and their relation to slow potentials. J. Physiol. (Lond.) 142, 1–21 (1958)
Westrum, L.E., Black, R.G.: Fine structural aspects of the synaptic organization of the spinal trigeminal nucleus (pars interpolaris) of the cat. Brain Res. 25, 265–288 (1971)
Wiesendanger, M., Hammer, B., Tarnecki, R.: Cortiocofugal control of presynaptic inhibition in the spinal trigeminal nucleus of the cat. The effect of pyramidotomy and barbiturates. Schweiz. Arch. Neurol. Neurochir. Psychiat. 100, 255–276 (1967)
Yu, H.H., Avery, J.K.: Primary afferent depolarization: direct evidence in the trigeminal system. Brain Res. 75, 328–333 (1974)
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Visiting investigator from Department of Physiology, Nippon Dental University, Niigata, Japan
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Nakamura, Y., Murakami, T., Kikuchi, M. et al. Primary afferent depolarization in the trigeminal spinal nucleus of cats. Exp Brain Res 29, 45–56 (1977). https://doi.org/10.1007/BF00236874
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DOI: https://doi.org/10.1007/BF00236874