Summary
Electrophysiological properties of neurones in the spinal cord dorsal horn were studied in decerebrated, immobilized spinal rats. Extracellular recordings were performed at the thoraco-lumbar junction level. Each track was systematically located by extracellular injection of pontamine sky blue. According to their responses to mechanical peripheral stimuli, cells were classified in four classes: Class 1 cells: Cells activated only by nonnoxious stimuli. They were divided into — 1A: hair movement and/or touch and 1B: hair movement and/or touch and pressure or pressure only. Class 2 cells: Cells driven by both nonnoxious and noxious stimuli, divided into — 2A: hair movement and/or touch, pressure, pinch and/or pin-prick, and 2B: pressure, pinch and/or pin-prick. Class 3 cells: Cells only activated by noxious stimuli (pinch and/or pin-prick). Class 4 cells: Cells responding to joint movement or pressure on deep tissues.
Peripheral transcutaneous or sural nerve stimulation clearly showed that class 1 cells were activated only by A fiber input while 68% of classes 2 and 3 cells received A and C input. Histological examination indicated that cells driven only by noxious input were located either in the deepest part or in the marginal zone (lamina I) of the dorsal horn. Nevertheless, some lamina I cells were also driven by both nonnoxious and noxious stimuli. In addition, there is a great deal of overlap between class 1 and class 2 cells. This fact was confirmed by considering the wide distribution in the dorsal horn of cells receiving A and C input. However, spinal organization of the different classes of cells consists of a preferential distribution rather than a strict lamination. This study indicates that properties of dorsal horn interneurones in the rat have a high degree of similarity with those previously described in other species (cat and monkey).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albe-Fessard, D., Levante, A., Lamour, Y.: Origin of spinothalamic and spinoreticular pathways in cats and monkeys. In: Advances in Neurology. Vol. 4: Pain (ed. J.J. Bonica), pp. 157–166. New York: Raven Press 1974
Applebaum, A.E., Beall, J.E., Foreman, R.D., Willis, W.D.: Organization and receptive fields of primate spinothalamic tract neurons. J. Neurophysiol. 38, 572–586 (1975)
Besson, J.M., Conseiller, C., Hamann, K.F., Maillard, M.G: Modifications of dorsal horn cell activities in the spinal cord, after intra-arterial injection of bradykinin. J. Physiol. (Lond.) 221, 189–205 (1972)
Bessou, P., Burgess, P.R., Perl, E.R., Taylor, C.B.: Dynamic properties of mechanoreceptors with unmyelinated (C) fibers. J. Neurophysiol. 34, 116–131 (1971)
Brown, A.G.: Effects of descending impulses on transmission through the spinocervical tract. J. Physiol. (Lond.) 219, 103–125 (1971)
Brown, A.G., Franz, D.N.: Responses of spinocervical tract neurons to natural stimulation of identified cutaneous receptors. Brain Res. 7, 231–249 (1969)
Brown, A.G., Hamann, W.C., Martin, H.F., III: Effects of activity in non-myelinated afferent fibres on the spinocervical tract. Brain Res. 98, 243–259 (1975)
Brown, P.B.: Response of cat dorsal horn cells to variations of intensity, location, and area of cutaneous stimuli. Exp. Neurol. 23, 249–265 (1975)
Brown, P.B., Fuchs, J.L.: Somatotopic representation of hindlimb skin in cat dorsal horn. J. Neurophysiol. 33, 1–9 (1975)
Brown, P.B., Fuchs, J.L., Tapper, D.N.: Parametric studies of dorsal horn neurons responding to tactile stimulation. J. Neurophysiol. 38, 19–25 (1975)
Bryan, R.N., Trevino, D.L., Coulter, J.D., Willis, W.D.: Location and somatotopic organization of the cells of origin of the spinocervical tract. Exp. Brain Res. 17, 177–189 (1973)
Bryan, R.N., Coulter, J.D., Willis, W.D.: Cells of origin of the spinocervical tract in the monkey. Exp. Neurol. 42, 574–586 (1974)
Cervero, F., Iggo, A., Ogawa, H.: Nociceptor driven dorsal horn neurones in the lumbar spinal cord of the cat. Pain 2, 5–24 (1976)
Christensen, B.N., Perl, E.R.: Spinal neurons specifically excited by noxious or thermal stimuli: the marginal zone of the dorsal horn. J. Neurophysiol. 33, 293–307 (1970)
Fetz, E.E.: Pyramidal tract effects on interneurons in the cat lumbar dorsal horn. J. Neurophysiol. 31, 69–80 (1968)
Foreman, R.D., Applebaum, A.E., Beall, J.E., Trevino, D.L., Willis, W.D.: Responses of primate spinothalamic tract neurons to electrical stimulation of hindlimb peripheral nerves. J. Neurophysiol. 38, 132–145 (1975)
Freminet, A., Bursaux, E., Poyart, C.: Mesure de la vitesse de renouvellement du lactate chez le rat par perfusion de 14 CU (L) lactate+. Pflügers Arch. 334, 293–302 (1972)
Fukushima, K., Kato, M.: Spinal interneurons responding to group II muscle afferent fibers in the cat. Brain Res. 90, 307–312 (1975)
Georgopoulos, A.P.: Functional properties of primary afferent units probably related to pain mechanisms in primate glabrous skin. J. Neurophysiol. 39, 71–83 (1976)
Gregor, M., Zimmermann, M.: Characteristics of spinal neurons responding to cutaneous myelinated and unmyelinated fibres. J. Physiol. (Lond.) 221, 555–576 (1972)
Hancock, M.B., Foreman, R.D., Willis, W.D.: Convergence of visceral and cutaneous input onto spinothalamic tract cells in the thoracic spinal cord of the cat. Exp. Neurol. 47, 240–248 (1975)
Handwerker, H.O., Iggo, A., Zimmermann, M.: Segmental and supraspinal actions on dorsal horn neurons responding to noxious and nonnoxious skin stimuli. Pain 1, 147–165 (1975)
Heavner, J.E., De Jong, R.H.: Spinal cord neuron response to natural stimuli. A microelectrode study. Exp. Neurol. 39, 293–306 (1973)
Hellon, R.F., Misra, N.K.: Neurones in the dorsal horn responding to scrotal skin temperature changes. J. Physiol. (Lond.) 232, 375–388 (1973)
Hillman, P., Wall, P.D.: Inhibitory and excitatory factors influencing the receptive fields of lamina V spinal cord cells. Exp. Brain Res. 9, 284–306 (1969)
Hongo, T., Jankowska, E., Lundberg, A.: Post-synaptic excitation and inhibition from primary afferents in neurones in the spinocervical tract. J. Physiol. (Lond.) 199, 569–592 (1968)
Iggo, A.: Cutaneous mechanoreceptors with afferent C fibers. J. Physiol. (Lond.) 152, 337–353 (1960)
Iggo, A.: Activation of cutaneous nociceptors and their actions on dorsal horn neurons. In: Advances in Neurology. Vol. 4: Pain (ed. J.J. Bonica), pp. 1–9. New York: Raven Press 1974
Iggo, A., Ramsey, R.L.: Dorsal horn neurones excited by cutaneous cold receptors in primates. J. Physiol. (Lond.) 242, 132–133 (1974)
Kolmodin, G.M., Skoglund, C.R.: Analysis of spinal interneurons activated by tactile and nociceptive stimulation. Acta physiol. scand. 50, 337–355 (1960)
Kumazawa, T., Perl, E.R., Burgess, P.R., Whitehorn, D.: Ascending projections from marginal zone (lamina I) neurons of the spinal dorsal horn. J. comp. Neurol. 162, 1–12 (1975)
Levante, A., Lamour, Y., Guilbaud, G., Besson, J.M.: Spinothalamic cell activity in the monkey during intense nociceptive stimulation: intra-arterial injection of bradykinin into the limbs. Brain Res. 88, 560–564 (1975)
Mendell, L.M.: Physiological properties of unmyelinated fibers projections to the spinal cord. Exp. Neurol. 16, 316–332 (1966)
Merrill, E.G., Wall, P.D.: Factors forming the edge of a receptive field: the presence of relatively ineffective afferent terminals. J. Physiol. (Lond.) 226, 825–846 (1972)
Pomeranz, G., Wall, P.D., Weber, W.V.: Cord cells responding to fine myelinated afferents from viscera, muscle and skin. J. Physiol. (Lond.) 199, 511–532 (1968)
Price, D.D., Browe, A.C.: Responses of spinal cord neurons to graded noxious and nonnoxious stimuli. Brain Res. 64, 425–429 (1973)
Price, D.D., Browe, A.C.: Spinal cord coding of graded nonnoxious and noxious temperature increases. Exp. Neurol. 48, 201–221 (1975)
Price, D.D., Hull, C.D., Buchwald, N.A.: Intracellular responses of dorsal horn cells to cutaneous and sural nerve A and C fiber stimuli. Exp. Neurol. 33, 291–309 (1971)
Price, D.D., Mayer, D.J.: Physiological laminar organization of the dorsal horn of M. mulatta. Brain Res. 79, 321–325 (1974)
Price, D.D., Mayer, D.J.: Neurophysiological characterization of the anterolateral quadrant neurons subserving in M. mulatta. Pain 1, 59–72 (1975)
Price, D.D., Wagman, I.H.: Physiological roles of A and C fiber inputs to the spinal dorsal horn of Macaca mulatta. Exp. Neurol. 29, 383–399 (1970)
Price, D.D., Wagman, I.H.: Relationship between pre- and post-synaptic effects of A and C fiber inputs to dorsal horn of M. mulatta. Exp. Neurol. 40, 90–103 (1973)
Selzer, M., Spencer, W.A.: Convergence of visceral and cutaneous afferent pathways in the lumbar spinal cord. Brain Res. 14, 331–348 (1969)
Steiner, T.J., Turner, L.M.: Cytoarchitecture of the rat spinal cord. J. Physiol. (Lond.) 222, 123–125P (1972)
Taub, A.: Local, segmental and supraspinal interaction with a dorsolateral spinal cutaneous afferent system. Exp. Neurol. 10, 357–374 (1964)
Wagman, I.H., Price, D.D.: Responses of dorsal horn cells of M. mulatta to cutaneous and sural nerve A and C fiber stimuli. J. Neurophysiol. 32, 803–817 (1969)
Wall, P.D.: Cord cells responding to touch, damage, and temperature skin. J. Neurophysiol. 23, 197–210 (1960)
Wall, P.D.: The laminar organization of dorsal horn cells and effects of descending impulses. J. Physiol. (Lond.) 188, 403–423 (1967)
Wall, P.D., Freeman, J., Major, D.: Dorsal horn cells in spinal and in freely moving rats. Exp. Neurol. 19, 519–529 (1967)
Willis, W.D., Trevino, D.L., Coulter, J.D., Maunz, R.A.: Response of primate spinothalamic tract neurons to natural stimulation of hindlimb. J. Neurophysiol. 37, 358–372 (1974)
Author information
Authors and Affiliations
Additional information
This work was supported by the C.N.R.S. (E.R.A. 237).
Rights and permissions
About this article
Cite this article
Menétrey, D., Giesler, G.J. & Besson, J.M. An analysis of response properties of spinal cord dorsal horn neurones to nonnoxious and noxious stimuli in the spinal rat. Exp Brain Res 27, 15–33 (1977). https://doi.org/10.1007/BF00234822
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00234822