Experimental Brain Research

, Volume 83, Issue 2, pp 385–396 | Cite as

Sensory neurons and motoneurons of the jaw-closing reflex pathway in rats: a combined morphological and physiological study using the intracellular horseradish peroxidase technique

  • K. Lingenhöhl
  • E. Friauf
Article

Summary

Motoneurons and muscle spindle afferents of the rat masseter muscle were physiologically and morphologically characterized. Their soma-dendritic morphology and axonal course were investigated using the intracellular horseradish peroxidase method. Following electrical stimulation of the masseter nerve, individual motoneurons were identified by antidromic all-or-none action potentials and individual sensory neurons by orthodromic action potentials. Using threshold separation an excitatory input from muscle spindles to a masseter motoneuron was demonstrated. The short latency difference of 0.34 ms between the mean orthodromic response in the sensory neurons and the beginning of the synaptic potential in the masseter motoneuron suggests a monosynaptic connection between the spindle afferents and the motoneurons. Following intrasomatic horse-radish peroxidase injection large multipolar cell bodies of masseter motoneurons were found within the motor nucleus. Their positions corresponded to the topographic organization of the motor trigeminal nucleus as described in retrograde tracing studies. Dendrites of masseter motoneurons were complex and could be found far beyond the nuclear borders. Distal dendrites extended to the mesencephalic trigeminal nucleus, the supratrigeminal nucleus, the lateral lemniscus and the reticular formation. Within the reticular formation dendrites were seen in the intertrigeminal nucleus and the peritrigeminal zone. Unipolar cell bodies of muscle spindle afferents were found in the mesencephalic trigeminal nucleus after intra-axonal injection of horseradish peroxidase. For all reconstructed sensory neurons a similar axonal course was found. Axonal terminals were found ipsilateral in the motor trigeminal nucleus, indicating a direct connection between sensory neurons and motoneurons. Further collaterals were found ipsilateral in the supratrigeminal nucleus and caudal to the motor trigeminal nucleus in the parvocellular reticular nucleus alpha. Since the latter termination areas are important for bilateral control of jaw-movements, the muscle spindle afferents are likely to participate not only in a monosynaptic motor reflex, but also in more complex neuronal circuits involved in jaw-movements.

Key words

Cranial motor reflex Masseter Morphology Physiology Trigeminal Rat 

Abbreviations

EPSP

excitatory postsynaptic potential

HRP

horseradish peroxidase

Me5

mesencephalic trigeminal nucleus

Mo5

motor trigeminal nucleus

PCRtA

parvocellular reticular nucleus alpha

Su5

supratrigeminal nucleus

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams JC (1981) Heavy metal intensification of DAB-based reaction product. J Histochem Cytochem 29:775Google Scholar
  2. Alvarado-Mallart MR, Batini C, Buisseret-Delmas C, Corvisier J (1975) Trigeminal representations of the masticatory and extraocular proprioceptors as revealed by horseradisch peroxidase retrograde transport. Brain Res 23:167–179Google Scholar
  3. Appenteng K, O'Donovan MJ, Somjen G, Stephens JA, Taylor A (1978) The projection of jaw elevator muscle spindle afferents to fifth nerve motoneurones in the cat. J Physiol (Lond) 279:409–423Google Scholar
  4. Appenteng K, Donga R, Willams RG (1985) Morphological and electrophysiological determination of the projections of jawelevator muscle spindle afferents in rats. J Physiol (Lond) 369:93–113Google Scholar
  5. Brown AG, Fyffe REW (1978) The morphology of group Ia afferent fibre collaterals in the spinal cord of the cat. J Physiol (Lond) 274:111–127Google Scholar
  6. Brown AG, Fyffe REW (1984) Intracellular staining of mammalian neurons: biological techniques series. Academic Press Inc, LondonGoogle Scholar
  7. Capra NF, Wax TD (1989) Distribution and central projections of primary afferent neurons that innervate the masseter muscle and mandibular periodontium: a double-label study. J Comp Neurol 279:341–352Google Scholar
  8. Cody FWJ, Lee RWH, Taylor A (1972) A functional analysis of the components of the mesencephalic nucleus of the fifth nerve in the cat. J Physiol (Lond) 226:249–261Google Scholar
  9. Coombs JS, Curtis DR, Eccles JC (1957) The interpretation of spike potentials of motoneurons. J Physiol (Lond) 139:198–231Google Scholar
  10. DeSantis M, Limwongse V, Rigamonti D (1978) Somatotopy in the trigeminal motor nucleus of the rat: field potentials recorded in the neuron pool after retrograde transport of horseradisch peroxidase. Neurosci Lett 10:95–98Google Scholar
  11. Dessem D, Taylor A (1989) Morphology of jaw-muscle spindle afferents in the rat. J Comp Neurol 282:389–403Google Scholar
  12. Friauf E (1986) Morphology of motoneurons in different subdivisions of the rat facial nucleus stained intracellularly with horseradish peroxidase. J Comp Neurol 253:231–241Google Scholar
  13. Fyffe REW (1979) The morphology of group II muscle afferent fibre collaterals. J Physiol (Lond) 296:39PGoogle Scholar
  14. Goldberg LJ, Chandler SH, Tal M (1982) Relationship between jaw movements and trigeminal motoneuron membranepotential fluctuations during cortically induced rhythmical jaw movements in the guinea pig. J Neurophysiol 48:110–125Google Scholar
  15. Holstege G, Kuypers HGJM, Dekker JJ (1977) The organization of the bulbar fibre connections to the trigeminal, facial and hypoglossus motor nuclei. Brain 100:265–286Google Scholar
  16. Hugelin A, Bonvallet M (1957) Etude oscillographique d'un réflexe monosynaptique crânien (réflexe massétérin). J Physiol (Paris) 49:210–211Google Scholar
  17. Inoue H, Moromoto T, Kawamura Y (1981) Response characteristics and classification of muscle spindles of the masseter muscle in the cat. Exp Neurol 74:548–560Google Scholar
  18. Itoh K, Konishi A, Nomura S, Mizuno N, Nakamura Y, Sugimoto T (1979) Application of coupled oxidation reaction to electron microscopic demonstration of horseradish peroxidase: cobalt-glucose method. Brain Res 175:341–346Google Scholar
  19. Jacquin MF, Rhoades RW, Enfiejian HL, Egger MD (1983) Organization and morphology of masticatory neurons in the rat: a retrograde HRP study. J Comp Neurol 218:239–256Google Scholar
  20. Jerge CR (1963a) Organization and function of the trigeminal mesencephalic nucleus. J Neurophysiol 26:379–392Google Scholar
  21. Jerge CR (1963b) The function of the nucleus supratrigeminalis. J Neurophysiol 26:393–402Google Scholar
  22. Kidokoro Y, Kubota K, Shuto S, Sumino R (1968) Reflex organization of cat masticatory muscles. J Neurophysiol 31:695–708Google Scholar
  23. Limwongse V, DeSantis M (1977) Cell body locations and axonal pathways of neurons innervating muscles of mastication in the rat. Am J Anat 149:477–488Google Scholar
  24. Lynch R (1985) A qualitative investigation of the topographical representation of masticatory muscles within the motor trigeminal nucleus of the rat: a horseradish peroxidase study. Brain Res 327:354–358Google Scholar
  25. Matesz C (1981) Peripheral and central distribution of fibres of the mesencephalic trigeminal root in the rat. Neurosci Lett 27:13–17Google Scholar
  26. Miyazaki R, Luschei ES (1987) Responses of neurons in the supratrigeminalis to sinusiodal jaw movements in the cat. Exp Neurol 96:145–157Google Scholar
  27. Mizuno N, Sauerland EK (1970) Trigeminal proprioceptive projections to the hypoglossus nucleus and the cervical ventral gray column. J Comp Neurol 139:215–226Google Scholar
  28. Mizuno N, Konishi A, Sato M (1975) Localization of masticatory motoneurons in the cat and rat by means of retrograde axonal transport of horseradish peroxidase. J Comp Neurol 164:105–116Google Scholar
  29. Moriyama Y (1987) Rhythmical jaw movements and lateral pontomedullary reticular neurons in rats. Comp Biochem Physiol 86:7–14Google Scholar
  30. Nomura S, Mizuno N (1983) Axonal trajectories of masticatory motoneurons: a genu formation of axons of jaw-opening motoneurons in the cat. Neurosci Lett 37:11–15Google Scholar
  31. Nomura S, Mizuno N (1985) Differential distribution of cell bodies and central axons of mesencephalic trigeminal nucleus neurons supplying the jaw-closing muscles and peridontal tissue: a transganglionic tracer study in the cat. Brain Res 359:311–319Google Scholar
  32. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, SydneyGoogle Scholar
  33. Rokx JTM, van Willigen JD (1985) Arrangement of supramandibular and suprahyoid motoneurons in the rat: a fluorescent tracer study. Acta Anat 122:158–162Google Scholar
  34. Rokx JTM, Jüch PJW, van Willigen JD (1986a) Arrangement and connections of mesencephalic trigeminal neurons in the rat. Acta Anat 127:7–15Google Scholar
  35. Rokx JTM, van Willigen JD, Jüch PWJ (1986b) Bilateral brainstem connections of the rat supratrigeminal region. Acta Anat 127:16–21Google Scholar
  36. Ruggiero DA, Ross CA, Kumada M, Reis DJ (1982) Reevaluation of projections from the mesencephalic trigeminal nucleus to the medulla and spinal cord new projections: a combined retrograde and anterograde horseradish peroxidase study. J Comp Neurol 206:278–292Google Scholar
  37. Sasamoto K (1979) Motor nuclear representation of masticatory muscles in the rat. Jpn J Physiol 29:739–747Google Scholar
  38. Shigenaga Y, Yoshida A, Tsuru K, Mitsuhiro Y, Otani K, Cao CQ (1988a) Physiological and morphological characteristics of cat masticatory motoneurons: intracellular injection of HRP. Brain Res 461:238–256Google Scholar
  39. Shigenaga Y, Mitsuhiro Y, Yoshida A, Cao CQ, Tsuru H (1988b) Morphology of single mesencephalic trigeminal neurons innervating masseter muscle of the cat. Brain Res 445:392–399Google Scholar
  40. Székely G, Matesz C (1982) The accessory motor nuclei of the trigeminal, facial, and abducens nerves in the rat. J Comp Neurol 210:258–264Google Scholar
  41. Szentágothai J (1948) Anatomical considerations of monosynaptic reflex arcs. J Neurophysiol 11:445–454Google Scholar
  42. Takata M, Kawamura Y (1970) Neurophysiologic properties of the supratrigeminal nucleus. Jpn J Physiol 20:1–11Google Scholar
  43. Travers JB, Norgren R (1983) Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280–298Google Scholar
  44. Yassin IBHM, Leong SK (1979) Location of neurons supplying the temporalis muscle in the rat and monkey. Neurosci Lett 11:63–68Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • K. Lingenhöhl
    • 1
  • E. Friauf
    • 1
  1. 1.Department of Animal PhysiologyUniversity of TübingenTübingen 1Germany

Personalised recommendations