Skip to main content

Synaptic interactions of retrogradely labeled hypoglossal motoneurons with substance P-like immunoreactive nerve terminals in the cat: a dual-labeling electron microscopic study

Experimental Brain Research volume 110, pages 175–182 (1996)Cite this article

Abstract

This study has investigated the synaptic interactions between hypoglossal motoneurons and substance P (SP)-immunoreactive terminals. Cholera toxin B conjugated to horseradish peroxidase was injected into the tip of the tongue on the right side of six ketamine-anesthetized cats. Two to five days later, the animals were killed. Cells containing HRP were labeled with a histochemical reaction utilizing tetramethylbenzidine (TMB) as the chromogen. TMB forms crystalline reaction products that are very distinct at the electron microscopic level. The tissues were then processed for immunocytochemisty using an antiserum against SP. The chromogen used in this case, di-aminobenzidine, yields amorphous reaction products. At the light microscopic level, labeled cells were observed primarily ipsilaterally in both intermediate and ventrolateral subdivisions of the hypoglossal nucleus. The majority of these labeled cells were seen at the level of obex. At the electron microscopic level, both asymmetric and symmetric synapses were observed. SP-immunoreactive nerve terminals formed asymmetric synapses with labeled dendrites and symmetric synapses with labeled perikarya. SP-labeled terminals also synapsed on unlabeled dendrites and somata. These are the first ultrastructural studies demonstrating synaptic interactions between hypoglossal motoneurons and SP terminals. These studies demonstrate that hypoglossal motoneurons that innervate intrinsic tongue muscles are modulated by SP and that SP may play a role in the control of fine movements of the tongue.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Abd-el-Malek S (1938) A contribution to the study of the movements of the tongue in animals, with special reference to the cat. J Anat 73:15–30

    Google Scholar 

  • Aldes LD, Chronister RB, Marco LA (1988a) Distribution of glutamic acid decarboxylase and gamma-aminobutyric acid in the hypoglossal nucleus in the rat. J Neurosci Res 19:343–348

    Google Scholar 

  • Aldes LD, Chronister RB, Shelton C, Haycock JW, Marco LA, Wong DL (1988b) Catecholamine innervation of the rat hypoglossal nucleus. Brain Res Bull 21:305–312

    Google Scholar 

  • Aldes LD, Chronister RC, Marco LA, Haycock JW, Thibault J (1988c) Differential distribution of biogenic amines in the hypoglossal nucleus of the rat. Exp Brain Res 73:305–314

    Google Scholar 

  • Aldes LD, Marco LA, Chronister RB (1989) Serotonin-containing axon terminals in the hypoglossal nucleus of the rat. An immuno-electronmicroscopic study. Brain Res Bull 23:249–256

    Google Scholar 

  • Aldes LD, Shaw B, Chronister RB, Haycock JW (1990) Catechol-amine-containing axon terminals in the hypoglossal nucleus of the rat: an immuno-electronmicroscopic study. Exp Brain Res 81:167–178

    Google Scholar 

  • Altschuler SM, Bao X, Miselis RR (1994) Dendritic architecture of hypoglossal motoneurons projecting to extrinsic tongue musculature in the rat. J Comp Neurol 342:538–550

    Google Scholar 

  • Arita H, Sakamoto M, Hirokawa Y, Okado N (1993) Serotonin innervation patterns differ among the various medullary moto-neuronal groups involved in upper airway control. Exp Brain Res 95:100–110

    Google Scholar 

  • Barnard JW (1940) The hypoglossal complex of vertebrates. J Comp Neurol 72:489–524

    Google Scholar 

  • Basbaum AI, Clanton CH, Fields HL (1978) Three bulbospinal pathways from the rostral medulla of the cat: an autoradiographic study of pain modulating mechanisms. J Comp Neurol 178:209–224

    Google Scholar 

  • Berger AJ, Bayliss DA, Viana F (1992) Modulation of neonatal rat hypoglossal motoneuron excitability by serotonin. Neurosci Lett 143:164–168

    Google Scholar 

  • Bobillier P, Seguin S, Petitjean F, Salvert D, Touret M, Jouvet M (1976) The raphe nuclei of the cat brainstem: a topographical atlas of their efferent projections as revealed by autoradiography. Brain Res 113:449–486

    Google Scholar 

  • Boone TB, Aldes LD (1984) The ultrastructure of two distinct neuron populations in the hypoglossal nucleus of the rat. Exp Brain Res 54:321–326

    Google Scholar 

  • Borke RC, Nau ME, Ringler RL (1983) Brain stem afferents of hypoglossal neurons in the rat. Brain Res 269:47–55

    Google Scholar 

  • Chan-Palay V (1982) Immunocytochemical and autoradiographic methods to demonstrate the coexistence of neuroactive substances: cerebellar Purkinje cells have glutamic acid decarboxylase and motilin immunoreactivity, and raphe neurons have serotonin and substance P immunoreactivity. In: Chan-Palay V, Palay SL (eds) Cytochemical methods in neuroanatomy. Liss, New York, pp 93–118

    Google Scholar 

  • Connaughton M, Priestley JV, Sofroniew MV, Eckenstein NF, Cuello AC (1986) Inputs to motoneurones in the hypoglossal nucleus of the rat: light and electron microscopic immunocyto-chemistry for choline acetyltransferase, substance P and enkephalins using monoclonal antibodies. Neuroscience 17:205–224

    Google Scholar 

  • Cooper MH (1981) Neurons of the hypoglossal nucleus of the rat. Otolaryngol Head Neck Surg 89:10–15

    Google Scholar 

  • Cuello AC, Kanazawa (1978) The distribution of substance P immunoreactive fibers in the rat central nervous system. J Comp Neurol 178:129–156

    Google Scholar 

  • Gatti PJ, Johnson TA, Shirahata M, Massari VJ (1994) Synaptic interactions of substance P immunoreactive (SP) nerve terminals with hypoglossal (N.XII) motoneurons which innervate the intrinsic muscles of the tongue: an electron microscopic dual labeling study. Soc Neurosci Abstr 20:1588

    Google Scholar 

  • Helke C, Charlton CG, Wiley RG (1985) Suicide transport of ricin demonstrates the presence of substance P receptors on medullary somatic and autonomic motor neurons. Brain Res 328:190–195

    Google Scholar 

  • Krammer EB, Rath T, Lischka MF (1979) Somatotopic organization of the hypoglossal nucleus: a HRP study in the rat. Brain Res 170:533–537

    Google Scholar 

  • Kubin L, Tojima H, Davies RO, Pack AI (1992) Serotonergic excitatory drive to hypoglossal motoneurons in the decerebrate cat. Neurosci Lett 139:243–248

    Google Scholar 

  • Larsson LI (1981) A novel immunocytochemical model system for specificity and sensitivity screening of antisera against multiple antigens. J Histochem Cytochem 29:408–410

    Google Scholar 

  • Li Y, Takada M, Mizuno N (1993) The sites of origin of serotoninergic afferent fibers in the trigeminal motor, facial and hypoglossal nuclei in the rat. Neurosci Res 17:307–313

    Google Scholar 

  • Ljungdahl A, Hokfelt T, Nilsson G (1978) Distribution of substance P-like immunoreactivity in the central nervous system of the rat. I. Cell bodies and nerve terminals. Neuroscience 3:861–943

    Article  CAS  PubMed  Google Scholar 

  • Llewellyn-Smith IJ, Pilowsky P, Minson JB (1993) The tungstate stabilized tetramethylbenzidine reaction for light and electron microscopic immunocytochemistry and for revealing biocytin-filled neurons. J Neurosci Methods 26:27–40

    Google Scholar 

  • Manaker S, Rizio G (1989) Autoradiographic localization of thyrotropin-releasing hormone and substance P receptors in the rat dorsal vagal complex. J Comp Neurol 290:516–526

    Google Scholar 

  • Manaker S, Tischler LJ (1993) Origin of serotoninergic afferents to the hypoglossal nucleus in the rat. J Comp Neurol 334:466–476

    Google Scholar 

  • Manaker S, Tischler LJ, Morrison AR (1992) Raphespinal and reticulospinal axon collaterals to the hypoglossal nucleus in the rat. J Comp Neurol 322:68–78

    Google Scholar 

  • Massari VJ, Johnson TA, Llewellyn-Smith IJ, Gatti PJ (1994) Ultrastructural interactions of substance P nerve terminals with negative chronotropic cardio-inhibitory neurons in the nucleus ambiguus. Brain Res 660:275–287

    Google Scholar 

  • Miyazaki T, Yoshida Y, Hirano M, Shin T, Kanaseki T (1981) Central location of the motoneurons supplying the thyrohyoid and the geniohyoid muscles as demonstrated by horseradish peroxidase method. Brain Res 219:423–427

    Google Scholar 

  • Morin D, Monteau R, Hilaire G (1992) Compared effects of serotonin on cervical and hypoglossal inspiratory activities: an in vitro study in the newborn rat. J Physiol (Lond) 451:605–629

    Google Scholar 

  • Nakaya Y, Kaneko T, Shigemoto R, Nakanishi S, Mizuno N (1994) Immunohistochemical localization of substance P receptor in the central nervous system of the adult rat. J Comp Neurol 347:249–274

    Google Scholar 

  • Odutola AB (1976) Cell grouping and Golgi architecture of the hypoglossal nucleus of the rat. Exp Neurol 52:356–371

    Google Scholar 

  • Peters A, Palay SL, Webster HDeF (1990) The fine structure of the nervous system. Oxford, New York, Oxford

    Google Scholar 

  • Shults CW, Quirion R, Chronwall B, Chase TN, O'Donohue TL (1984) A comparison of the anatomical distribution of substance P and substance P receptors in the rat central nervous system. Peptides 5:1097–1128

    Google Scholar 

  • Sokoloff AJ (1991) Musculotopic organization of the hypoglossal nucleus in the grass frog, Rana pipiens. J Comp Neurol 308:505–512

    Google Scholar 

  • Sonntag CF (1925) The comparative anatomy of the tongues of mammalia. XII. Summary, classification and physiology. J Zool Proc Zool Soc Lond 21:701–762

    Google Scholar 

  • Takada M, Itoh K, Yasui Y, Mitani A, Nomura S, Mizuno N (1984) Distribution of premotor neurons for the hypoglossal nucleus in the cat. Neurosci Lett 52:141–146

    Google Scholar 

  • Takeuchi Y, Kojima M, Matsuura T, Sano Y (1983) Serotonergic innervation on the motoneurons in the mammalian brainstem. Anat Embryol 167:321–333

    Google Scholar 

  • Travers JB, Norgren R (1983) Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280–298

    Google Scholar 

  • Uemura M, Matsuda K, Kume M, Takeuchi Y, Matsushima R, Mizuno N (1979) Topographical arrangement of hypoglossal motoneurons: an HRP study in the cat. Neurosci Lett 13:99–104

    Google Scholar 

  • Uemura-Sumi M, Mizuno N, Nomura S, Iwahori N, Takeuchi Y, Matsushima R (1981) Topographical representation of the hypoglossal nerve branches and tongue muscles in the hypoglossal nucleus of macaque monkeys. Neurosci Lett 22:31–35

    Google Scholar 

  • Uemura-Sumi M, Itoh M, Mizuno N (1988) The distribution of hypoglossal motoneurons in the dog, rabbit and rat. Anat Embryol (Berl) 177:389–394

    Google Scholar 

  • Wan XS, Trojanowski JQ, Gonatas JO, Liu CN (1982) Cytoarchitecture of the extranuclear and commissural dendrites of hypo-glossal nucleus neurons as revealed by conjugates of horseradish peroxidase with cholera toxin. Exp Neurol 78:167–175

    Google Scholar 

Download references

Author information

Affiliations

  1. Department of Pharmacology, Howard University College of Medicine, 520 “W” St., NW, 20059, Washington, DC, USA

    P. J. Gatti, W. C. Coleman & V. J. Massari

  2. Department of Environmental Health Science, Division of Physiology, Johns Hopkins Medical Institutes, Baltimore, Md., USA

    M. Shirahata

  3. Department of Veterinary Services, Howard University College of Medicine, Washington, D.C., USA

    T. A. Johnson

Authors
  1. P. J. Gatti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. C. Coleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Shirahata
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. A. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. V. J. Massari
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gatti, P.J., Coleman, W.C., Shirahata, M. et al. Synaptic interactions of retrogradely labeled hypoglossal motoneurons with substance P-like immunoreactive nerve terminals in the cat: a dual-labeling electron microscopic study. Exp Brain Res 110, 175–182 (1996). https://doi.org/10.1007/BF00228549

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00228549

Key words

  • Hypoglossal motoneurons
  • Retrograde transport
  • Synaptic interactions
  • Substance P
  • Cat