Axonal transport studies of the trigeminal nerve roots of the cat

With special reference to afferent contributions to the portio minor

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✓ The transport of protein molecules by axoplasmic flow has been used to trace axonal projections in the trigeminal system of the cat. Autoradiography with tritiated amino acid labeling of synthesized proteins and the transport of the enzyme horseradish peroxidase have been employed. The latter method has enabled demonstration of afferent axons within the portio minor, some of which are of cutaneous origin. The trigeminal “motor root” thus appears to be homologous with spinal ventral roots in possessing a potentially significant sensory function. The presence of such afferent fibers in nerve roots thought previously to have an exclusively motor function may explain instances of preserved sensation or failure to relieve pain following rhizotomy of the trigeminal portio major.

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Address reprint requests to: Ronald F. Young, M.D., Division of Neurosurgery, Harbor/UCLA Medical Center, 1000 West Carson Street, Torrance, California 90509.

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    Dark-field autoradiographs showing axonal transport labeling of “sensory” and “motor” fibers of the trigeminal roots in the cat. a: Injection of a mixture of 3H-leucine and 3H-proline into the Gasserian ganglion results in the massive transport of labeled axonal proteins in the portio major (top) and some evidence of linear silver grains in the portio minor (arrow) suggestive of labeled axons derived from ganglion cells. × 58. b: Injection of the same radioactive neuronal protein precursors in the pontine motor nucleus of the fifth nerve reveals axonal transport into the portio minor, which can be seen running its diagonal course across and below the unlabeled portio major, the latter totally lacking efferent fibers. × 13.

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    Axonal transport of the enzyme horseradish peroxidase from ophthalmic, maxillary, and mandibular nerve branches can be massively traced by histochemical reaction product into the trigeminal portio major (a), indicating its principal afferent role, but, in addition, isolated axons can also be identified in selected zones of the portio minor (b). × 112.

References

  • 1.

    Alvarado-Mallart MRBatini CBuisseret-Delmas Cet al: Trigeminal representations of the masticatory and extraocular proprioceptors as revealed by horseradish peroxidase retrograde transport. Exp Brain Res 23:1671791975Alvarado-Mallart MR Batini C Buisseret-Delmas C et al: Trigeminal representations of the masticatory and extraocular proprioceptors as revealed by horseradish peroxidase retrograde transport. Exp Brain Res 23:167–179 1975

  • 2.

    Christensen BNPerl ER: Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J Neurophysiol 33:2933071970Christensen BN Perl ER: Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J Neurophysiol 33:293–307 1970

  • 3.

    Coggeshall REApplebaum MLFazen Met al: Unmyelinated axons in human ventral roots, a possible explanation for the failure of dorsal rhizotomy to relieve pain. Brain 98:1571661975Coggeshall RE Applebaum ML Fazen M et al: Unmyelinated axons in human ventral roots a possible explanation for the failure of dorsal rhizotomy to relieve pain. Brain 98:157–166 1975

  • 4.

    Coggeshall RECoulter JDWillis WD Jr: Unmyelinated axons in the ventral roots of the cat lumbosacral enlargement. J Comp Neurol 153:39581974Coggeshall RE Coulter JD Willis WD Jr: Unmyelinated axons in the ventral roots of the cat lumbosacral enlargement. J Comp Neurol 153:39–58 1974

  • 5.

    Coggeshall RECoulter JDWillis WD Jr: Unmyelinated fibers in the ventral root. Brain Res 57:2292331973Coggeshall RE Coulter JD Willis WD Jr: Unmyelinated fibers in the ventral root. Brain Res 57:229–233 1973

  • 6.

    Cowan WMGottlieb DIHendrickson AEet al: The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res 37:21511972Cowan WM Gottlieb DI Hendrickson AE et al: The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res 37:21–51 1972

  • 7.

    Dandy WE: An operation for the cure of tic douloureux: partial section of the sensory root at the pons. Arch Surg 18:6877341929Dandy WE: An operation for the cure of tic douloureux: partial section of the sensory root at the pons. Arch Surg 18:687–734 1929

  • 8.

    Denny-Brown DYanagisawa N: The function of the descending root of the fifth nerve. Brain 96:7838141973Denny-Brown D Yanagisawa N: The function of the descending root of the fifth nerve. Brain 96:783–814 1973

  • 9.

    Dimsdale JAKamp JM: Afferent fibers in the ventral roots of the rat. J Physiol 187:25P26P1966 (Proceedings)Dimsdale JA Kamp JM: Afferent fibers in the ventral roots of the rat. J Physiol 187:25P–26P 1966 (Proceedings)

  • 10.

    Feldman SGKruger L: An axonal transport study of the ascending projection of medial lemniscus in the rat. J Comp Neurol 192:4274541980Feldman SG Kruger L: An axonal transport study of the ascending projection of medial lemniscus in the rat. J Comp Neurol 192:427–454 1980

  • 11.

    Furstman LSaporta SKruger L: Retrograde axonal transport of horseradish peroxidase in sensory nerves and ganglion cells of the rat. Brain Res 84:3203241975Furstman L Saporta S Kruger L: Retrograde axonal transport of horseradish peroxidase in sensory nerves and ganglion cells of the rat. Brain Res 84:320–324 1975

  • 12.

    Gudmundsson KRhoton AL JrRushton JG: Detailed anatomy of the intracranial portion of the trigeminal nerve. J Neurosurg 35:5926001971Gudmundsson K Rhoton AL Jr Rushton JG: Detailed anatomy of the intracranial portion of the trigeminal nerve. J Neurosurg 35:592–600 1971

  • 13.

    Hodge CJ JrKing RB: Medical modification of sensation. J Neurosurg 44:21281976Hodge CJ Jr King RB: Medical modification of sensation. J Neurosurg 44:21–28 1976

  • 14.

    Hosobuchi Y: The majority of unmyelinated afferent axons in human ventral roots probably conduct pain. Pain 8:1671801980Hosobuchi Y: The majority of unmyelinated afferent axons in human ventral roots probably conduct pain. Pain 8:167–180 1980

  • 15.

    Jacob MWeddell G: Neural intersegmental connection in the spinal root and ganglion region of the rat. J Comp Neurol 161:1151231975Jacob M Weddell G: Neural intersegmental connection in the spinal root and ganglion region of the rat. J Comp Neurol 161:115–123 1975

  • 16.

    Kato MTanji J: Physiological properties of sensory fibers in the spinal ventral roots in the cat. Jpn J Physiol 21:71771971Kato M Tanji J: Physiological properties of sensory fibers in the spinal ventral roots in the cat. Jpn J Physiol 21:71–77 1971

  • 17.

    Kruger L: Functional subdivision of the brainstem sensory trigeminal nuclear complex. Adv Pain Res Ther 3:1972091979Kruger L: Functional subdivision of the brainstem sensory trigeminal nuclear complex. Adv Pain Res Ther 3:197–209 1979

  • 18.

    Kruger LSaporta SFeldman SG: Axonal transport studies of the sensory trigeminal complex in Anderson DJMatthews B (eds): Pain in the Trigeminal Region. New York: American Elsevier1977 pp 191201Kruger L Saporta S Feldman SG: Axonal transport studies of the sensory trigeminal complex in Anderson DJ Matthews B (eds): Pain in the Trigeminal Region.New York: American Elsevier 1977 pp 191–201

  • 19.

    Kumazawa TPerl ER: Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: indications of their place in dorsal horn functional organization. J Comp Neurol 177:4174341978Kumazawa T Perl ER: Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: indications of their place in dorsal horn functional organization. J Comp Neurol 177:417–434 1978

  • 20.

    Light ARMetz CB: The morphology of the spinal cord efferent and afferent neurons contributing to the ventral roots of the cat. J Comp Neurol 179:5015161978Light AR Metz CB: The morphology of the spinal cord efferent and afferent neurons contributing to the ventral roots of the cat. J Comp Neurol 179:501–516 1978

  • 21.

    Light ARPerl ER: Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186:1331501979Light AR Perl ER: Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186:133–150 1979

  • 22.

    Loeser JD: Dorsal rhizotomy for the relief of chronic pain. J Neurosurg 36:7457501972Loeser JD: Dorsal rhizotomy for the relief of chronic pain. J Neurosurg 36:745–750 1972

  • 23.

    Mesulam M-M: Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:1061171978Mesulam M-M: Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117 1978

  • 24.

    Onofrio BMCampa HK: Evaluation of rhizotomy. Review of twelve years' experience. J Neurosurg 40:7517551972Onofrio BM Campa HK: Evaluation of rhizotomy. Review of twelve years' experience. J Neurosurg 40:751–755 1972

  • 25.

    Pelletier VAPoulos DALende RA: Functional localization in the trigeminal root. J Neurosurg 40:5045131974Pelletier VA Poulos DA Lende RA: Functional localization in the trigeminal root. J Neurosurg 40:504–513 1974

  • 26.

    White JCSweet WH: Pain and the Neurosurgeon: A Forty Year Experience. Springfield, IL: Charles C Thomas1969 pp 648654White JC Sweet WH: Pain and the Neurosurgeon: A Forty Year Experience.Springfield IL: Charles C Thomas 1969 pp 648–654

  • 27.

    Young RF: Unmyelinated fibers in the trigeminal motor root. Possible relationship to the results of trigeminal rhizotomy. J Neurosurg 49:5385431978Young RF: Unmyelinated fibers in the trigeminal motor root. Possible relationship to the results of trigeminal rhizotomy. J Neurosurg 49:538–543 1978

  • 28.

    Young RFStevens R: Unmyelinated axons in the trigeminal motor root of human and cat. J Comp Neurol 183:2052141979Young RF Stevens R: Unmyelinated axons in the trigeminal motor root of human and cat. J Comp Neurol 183:205–214 1979

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