Skip to main content

Advertisement

Log in

Quantitative analysis of the dendritic architectures of single jaw-closing and jaw-opening motoneurons in cats

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Little is known about the dendritic architectures of trigeminal motoneurons innervating antagonistic muscles. Thus, the aim of the present study was to provide a quantitative description of jaw-closing (JC) and jaw-opening (JO) alpha motoneurons and to determine geometrical similarities and differences of the dendritic tree between the two. Seven JC alpha motoneurons and four JO alpha motoneurons were intracellulary labeled with horseradish peroxidase (HRP) in the cat and quantitatively analyzed with a computer-assisted three-dimensional system. The dendritic tree of JC alpha motoneurons was confined within the JC motor nucleus, despite locations of the cell body. In contrast, JO alpha motoneurons generated extensive extranuclear dendrites in the reticular formation. The branching pattern of proximal dendritic segments was simpler in the JC than in the JO alpha motoneurons. Despite these differences, the mean values of dendritic parameters examined per neuron were not different between the two kinds of alpha motoneurons, and the stem dendrite diameter was positively correlated with several dendritic parameters in a linear manner. The present study provides new evidence that underlying design principles of the geometry of the dendritic tree are not concerned with the differences in configuration and branching pattern of the dendritic tree of trigeminal alpha motoneurons innervating antagonistic muscles. In addition, we estimated the number of excitatory and inhibitory synapses covering dendrites of single JC alpha motoneurons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1A–E.
Fig. 2A, B.
Fig. 3A–D.
Fig. 4. A, B
Fig. 5A–C.
Fig. 6A–C.
Fig. 7.

Similar content being viewed by others

References

  • Bae YC, Choi BJ, Lee MG, Lee HJ, Park KP, Zhang LF, Honma S, Fukami H, Yoshida A, Ottersen OP, Shigenaga Y (2002) Quantitative ultrastructural analysis of glycine- and GABA-immunoreactive terminals on trigeminal alpha- and gamma-motoneuron somata in the rat. J Comp Neurol 422:308–319

    Article  Google Scholar 

  • Bae YC, Nakagawa S, Yabuta NH, Yoshida A, Pil PK, Moritani M, Chen K, Takemura M, Shigenaga Y (1996) Electron microscopic observations of synaptic connections of jaw-muscle spindle and periodontal afferent terminals in the trigeminal motor and supratrigeminal nuclei in the cat. J Comp Neurol 374:421–435

    Article  CAS  PubMed  Google Scholar 

  • Bae YC, Nakamura T, Ihn HJ, Choi MH, Yoshida A, Moritani M, Honma S, Shigenaga Y (1999) Distribution pattern of inhibitory and excitatory synapses in the dendritic tree of single masseter α-motoneurons in the cat. J Comp Neurol 414:454–468

    Google Scholar 

  • Brännström T (1993) Quantitative synaptology of functionally different types of cat medial gastrocnemius α-motoneurons. J Comp Neurol 330:439–454

    PubMed  Google Scholar 

  • Burke RE, Dum RP, Fleshman JW, Glenn LL, Lev-Tov A, O'Donovan MJ, Pinter MJ (1982) An HRP study of the relation between cell size and motor unit type in cat ankle extensor motoneurons. J Comp Neurol 209:17–28

    CAS  PubMed  Google Scholar 

  • Cameron WE, Averill DB, Berger AJ (1985) Quantitative analysis of the dendrites of cat phrenic motoneurons stained intracellularly with horseradish peroxidase. J Comp Neurol 230:91–101

    Google Scholar 

  • Capowski JJ (1989) Computer techniques in neuroanatomy. Plenum Press, New York

  • Chandler SH, Goldberg LJ (1982) Intracellular analysis of synaptic mechanisms controlling spontaneous and cortically induced jaw movements in the guinea pig. J Neurophysiol 48:126–138

    CAS  PubMed  Google Scholar 

  • Cullheim S, Fleshman JW, Glenn LL, Burke RE (1987) Membrane area and dendritic structure in type-identified triceps surae alpha motoneurons. J Comp Neurol 255:68–81

    CAS  PubMed  Google Scholar 

  • Fukunishi Y, Nagase Y, Yoshida A, Moritani M, Honma S, Hirose Y, Shigenaga Y (1999) Quantitative analysis of the dendritic architectures of cat hypoglossal motoneurons stained intracellularly with horseradish peroxidase. J Comp Neurol 405:345–358

    Article  CAS  PubMed  Google Scholar 

  • Goldberg LJ, Chandler SH, Tal M (1982) Relationship between jaw movements and trigeminal motoneuron membrane-potential fluctuations during cortically induced rhythmical jaw movements in the guinea pig. J Neurophysiol 48:110–125

    CAS  PubMed  Google Scholar 

  • Kernell D, Zwaagstra B (1989) Size and remoteness: two relatively independent parameters of dendrites, as studied for spinal motoneurones of the cat. J Physiol (Lond) 413:233–254

    Google Scholar 

  • Kidokoro Y, Kubota K, Shuto S, Sumino R (1968a) Reflex organization of cat masticatory muscles. J Neurophysiol 31:695–708

    CAS  PubMed  Google Scholar 

  • Kidokoro Y, Kubota K, Shuto S, Sumino R (1968b) Possible interneurons responsible for reflex inhibition of motoneurons of jaw-closing muscles from the inferior dental nerve. J Neurophysiol 31:709–716

    CAS  PubMed  Google Scholar 

  • Kubo Y, Enomoto S, Nakamura Y (1981) Synaptic basis of orbital cortically induced rhythmical masticatory activity of trigeminal motoneurons in immobilized cats. Brain Res 230:97–110

    CAS  PubMed  Google Scholar 

  • Nagase Y, Moritani M, Nakagawa S, Yoshida A, Takemura M, Zhang LF, Kida H, Shigenaga Y (1997) Serotonergic axonal contacts on identified cat trigeminal motoneurons and their correlation with medullary raphe nucleus stimulation. J Comp Neurol 384:443–455

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Kubo Y (1978) Masticatory rhythm in intracellular potentials of trigeminal motoneurons induced by stimulation of orbital cortex and amygdala in cats. Brain Res 148:504–509

    CAS  PubMed  Google Scholar 

  • Örnung G, Ottersen OP, Cullheim S, Ulfhake B (1998) Distribution of glutamate-, glycine- and GABA-immunoreactive nerve terminals on dendrites in the cat spinal motor nucleus. Exp Brain Res 118:517-532

    Article  PubMed  Google Scholar 

  • Örnung G, Shupliakov O, Linda H, Ottersen OP, Storm-Mathisen J, Ulfhake B, Cullheim S (1996) Qualitative and quantitative analysis of glycine- and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord: a postembedding electron microscopic study. J Comp Neurol 365:413-426

    Article  PubMed  Google Scholar 

  • Rall W (1977) Core conductor theory and cable properties of neurons. In: Kandel ER (ed) The nervous system (vol I). Cellular biology of neurons, part I. American Physiological Society, Washington DC, pp 39–97

  • Rose PK, Keirstesd SA, Vanner SJ (1985) A quantitative analysis of the geometry of cat motoneurons innervating neck and shoulder muscles. J Comp Neurol 239:89–107

    CAS  PubMed  Google Scholar 

  • Rose PK, Neuber-Hess M (1991) Morphology and frequency of axon terminals on the somata, proximal dendrites, and distal dendrites of dorsal neck motoneurons in the cat. J Comp Neurol 307:259–280

    CAS  PubMed  Google Scholar 

  • Russell-Mergenthal H, McClung JR, Goldberg SJ (1986) The determination of dendrite morphology on lateral rectus motoneurons in cat. J Comp Neurol 245:116–122

    CAS  PubMed  Google Scholar 

  • Shigenaga Y, Hirose Y, Yoshida A, Fukami H, Honma S, Bae YC (2000) Quantitative ultrastructure of physiologically identified premotoneuron terminals in the trigeminal motor nucleus in the cat. J Comp Neurol 426:13–30

    Article  CAS  PubMed  Google Scholar 

  • Shigenaga Y, Mitsuhiro Y, Shirana Y, Tsuru K (1990) Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP. Brain Res 514:219–237

    CAS  PubMed  Google Scholar 

  • Shigenaga Y, Doe K, Suemune S, Mitsuhiro Y, Tsuru K, Otani K, Shirana M, Hosoi M, Yoshida A, Kagawa K (1989) Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat: intra-axonal staining with HRP. Brain Res 505:91–110

    CAS  PubMed  Google Scholar 

  • Shigenaga Y, Yoshida A, Tsuru H, Mitsuhiro Y, Otani K, Cao CQ (1988) Physiological and morphological characteristics of cat masticatory motoneurons-intracellular injection of HRP. Brain Res 461:238–256

    CAS  PubMed  Google Scholar 

  • Turman JE Jr, Chopiuk NB, Shuler CF (2001) The Krox-20 null mutation differentially affects the development of masticatory muscles. Dev Neurosci 23:113–121

    CAS  PubMed  Google Scholar 

  • Ulfhake B, Cullheim S (1988) Postnatal development of cat hind limb motoneurons, III: changes in size of motoneurons supplying the triceps surae muscle. J Comp Neurol 278:103–120

    CAS  PubMed  Google Scholar 

  • Ulfhake B, Kellerth JO (1981) A quantitative light microscopic study of the dendrites of cat spinal α-motoneurons after intracellular staining with horseradish peroxidase. J Comp Neurol 202:571–583

    CAS  PubMed  Google Scholar 

  • Ulfhake B, Kellerth JO (1982) Does α-motoneurone size correlate with motor unit type in cat triceps surae? Brain Res 251:201–209

    CAS  PubMed  Google Scholar 

  • Ulfhake B, Kellerth JO (1983) A quantitative morphological study of HRP-labeled cat α-motoneurones supplying different muscles. Brain Res 264:1–20

    CAS  PubMed  Google Scholar 

  • Ulfhake B, Kellerth JO (1984) Electrophysiological and morphological measurements in cat gastrocnemius and soleus α-motoneurones. Brain Res 307:167–179

    CAS  PubMed  Google Scholar 

  • Yabuta NH, Yasuda K, Nagase Y, Yoshida A, Fukunishi Y, Shigenaga Y (1996) Light microscopic observation of the contacts made between two spindle afferent types and α-motoneurons in the cat trigeminal motor nucleus. J Comp Neurol 374:436–450

    Article  CAS  PubMed  Google Scholar 

  • Yoshida A, Fukami H, Nagase Y, Appenteng K, Honma S, Zhang LF, Bae YC, Shigenaga Y (2001) Quantitative analysis of synaptic contacts made between functionally identified oralis neurons and trigeminal motoneurons in cats. J Neurosci 21:6298–6307

    CAS  PubMed  Google Scholar 

  • Yoshida A, Mukai N, Moritani M, Nagase Y, Hirose Y, Honma S, Fukami H, Takagi K, Matsuya T, Shigenaga Y (1999) Physiologic and morphologic properties of motoneurons and spindle afferents innervating the temporal muscles in the cat. J Comp Neurol 406:29–50

    Google Scholar 

  • Yoshida A, Yasuda K, Dostrovsky JO, Bae YC, Takemura M, Shigenaga Y, Sessle BJ (1994) Two major types of premotoneurons in the feline trigeminal nucleus oralis neurons as demonstrated by intracellular staining with HRP. J Comp Neurol 347:495–514

    CAS  PubMed  Google Scholar 

  • Zwaagstra B, Kernell D (1981) Sizes of soma and stem dendrites in intracellularly labeled α-motoneurons of the cat. Brain Res 204:295–309

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This project was supported by the Ministry of Education, Science and Culture of Japan (Grant no. 10307044 to Y.S. and no. 13671899 to A.Y.). We gratefully thank Dr. Barry J. Sessle for his critical reading of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Atsushi Yoshida.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moritani, M., Kida, H., Nagase, Y. et al. Quantitative analysis of the dendritic architectures of single jaw-closing and jaw-opening motoneurons in cats. Exp Brain Res 150, 265–275 (2003). https://doi.org/10.1007/s00221-003-1458-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-003-1458-9

Keywords

Navigation