International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
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Quantitative Ultrastructural Analysis of Endings Presynaptic to the Tooth Pulp Afferent Terminals in the Trigeminal Oral Nucleus

  • Lee, Suk-Ki (Department of Anatomy and Neurobiology, School of Dentistry, Kyungpook National University) ;
  • Kim, Tae Heon (Department of Anatomy and Neurobiology, School of Dentistry, Kyungpook National University) ;
  • Lee, Cheon-Hee (Department of Dental Hygiene, Andong Science College) ;
  • Park, Sook Kyung (Department of Anatomy and Neurobiology, School of Dentistry, Kyungpook National University) ;
  • Bae, Yong Chul (Department of Anatomy and Neurobiology, School of Dentistry, Kyungpook National University)
  • Received : 2016.08.20
  • Accepted : 2016.09.10
  • Published : 2016.09.30
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Abstract

The ultrastructural parameters related to synaptic release of endings which are presynaptic to tooth pulp afferent terminals (p-endings) were analyzed to understand the underlying mechanism for presynaptic modulation of tooth pulp afferents. Tooth pulp afferents were labelled by applying wheat-germ agglutinin conjugated horseradish peroxidase to the rat right lower incisor, whereafter electron microscopic morphometric analysis with serial section and reconstruction of p-endings in the trigeminal oral nucleus was performed. The results obtained from 15 p-endings presynaptic to 11 labeled tooth pulp afferent terminals were as follows. P-endings contained pleomorphic vesicles and made symmetrical synaptic contacts with labeled terminals. The p-endings showed small synaptic release-related ultrastructural parameters: volume, $0.82{\pm}0.45{\mu}m^3$ ($mean{\pm}SD$); surface area, $4.50{\pm}1.76{\mu}m^2$; mitochondrial volume, $0.15{\pm}0.07{\mu}m^3$; total apposed surface area, $0.69{\pm}0.24{\mu}m^2$; active zone area, $0.10{\pm}0.04{\mu}m^2$; total vesicle number, $1045{\pm}668.86$; and vesicle density, $1677{\pm}684/{\mu}m^2$. The volume of the p-endings showed strong positive correlation with the following parameters: surface area (r=0.97, P<0.01), mitochondrial volume (r=0.56, P<0.05), and total vesicle number (r=0.73, P<0.05). However, the volume of p-endings did not positively correlate or was very weakly correlated with the apposed surface area (r=-0.12, P=0.675) and active zone area (r=0.46, P=0.084). These results show that some synaptic release-related ultrastructural parameters of p-endings on the tooth pulp afferent terminals follow the "size principle" of Pierce and Mendell (1993) in the trigeminal nucleus oralis, but other parameters do not. Our findings may demonstrate a characteristic feature of synaptic release associated with p-endings.

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References

  1. Olszewski J. On the anatomical and functional organization of the spinal trigeminal nucleus. J Comp Neurol. 1950;92:401-413. https://doi.org/10.1002/cne.900920305
  2. Yasui Y, Itoh K, Mizuno N, Nomura S, Takada M, Konishi A, Kudo M. The posteromedial ventral nucleus of the thalamus (VPM) of the cat: direct ascending projections to the cytoarchitectonic subdivisions. J Comp Neurol. 1983;220:219-228. https://doi.org/10.1002/cne.902200209
  3. Tsuru K, Otani K, Kajiyama K, Suemune S, Shigenaga Y. Central terminations of periodontal mechanoreceptive and tooth pulp afferents in the trigeminal principal and oral nuclei of the cat. Brain Res. 1989;485:29-61. https://doi.org/10.1016/0006-8993(89)90665-3
  4. Yoshida A, Hasuda K, Dostrovsky JO, Bae YC, Takemura M, Shigenaga Y, Sessle BJ. Two major types of premotoneurons in the feline trigeminal nucleus oralis neurons as demonstrated by intracellular stianing with HRP. J Comp Neurol. 1994;347:495-514. https://doi.org/10.1002/cne.903470403
  5. Shigenaga Y, Mitsuhiro Y, Yoshida A, Cao CQ, Tsuru H. Morphology of single mesencephalic trigeminal neurons innervating masseter muscle of the cat. Brain Res. 1988;445:392-399. https://doi.org/10.1016/0006-8993(88)91206-1
  6. Shigenaga Y, Yoshida A, Mitsuhiro H, Tsuru K, Doe K. Morphological and functional properties of trigeminal nucleus oralis neurons projecting to the trigeminal motor nucleus of the cat. Brain Res. 1988;416:143-149.
  7. Sugimoto T, He YF, Funahashi M, Ichikawa H. Induction of immediate-early genes c-fos and zif268 in the subnucleus oralis by noxious tooth pulp stimulation. Brain Res. 1998;794(2):353-358. https://doi.org/10.1016/S0006-8993(98)00333-3
  8. Sugimoto T, He YF, Xiao C, Ichikawa H. c-fos induction in the subnucleus oralis following trigeminal nerve stimulation. Brain Res. 1998;783(1):158-162. https://doi.org/10.1016/S0006-8993(97)01176-1
  9. Oakden EL, Boissonade FM. Fos expression in the ferret trigeminal nuclear complex following tooth pulp stimulation. Neuroscience. 1998;84(4):1197-1208. https://doi.org/10.1016/S0306-4522(97)00550-2
  10. Kiernan JA. Barr's the human nervous system, An anatomical viewpoint. 7th ed. Philadelphia: Lippincott-Raven; 1998. p. 157-162.
  11. Bae YC, Yoshida A. Ultrastructural basis for craniofacial sensory processing in the brainstem. Int Rev Neurobiol. 2011;97:99-141. doi: 10.1016/B978-0-12-385198-7.00005-9.Review.
  12. Nicol MJ, Walmsley B. A serial section electron microscope study of an identified Ia afferent collateral in the cat spinal cord. J Comp Neurol. 1991;314:257-277. https://doi.org/10.1002/cne.903140205
  13. Pierce JP, Mendell LM. Quantitative ultrastructure of Ia boutons in the ventral horn: scaling and positional relationships. J Neurosci. 1993;13:4748-4763. https://doi.org/10.1523/JNEUROSCI.13-11-04748.1993
  14. Nakagawa S, Kurata S, Yoshida A, Nagase Y, Moritani M, Takemura M, Bae YC, Shigenaga Y. Ultrastructural observations of synaptic connections of vibrissa afferent terminals in cat principal sensory nucleus and morphometry of related synaptic elements. J Comp Neurol. 1997;389(1):12-33. https://doi.org/10.1002/(SICI)1096-9861(19971208)389:1<12::AID-CNE2>3.0.CO;2-H
  15. Bae YC, Park KP, Yoshida A, Nakagawa S, Kurata S, Takemura M, Shigenaga Y. Identification of gamma aminobutyric acid (GABA)-immunoreactive axon endings associatied with periodontal mesenciphalic afferent terminals and morphometry of the two types of terminal in the cat supratrigeminal nucleus. J Comp Neurol. 1997;389:127-138. https://doi.org/10.1002/(SICI)1096-9861(19971208)389:1<127::AID-CNE9>3.0.CO;2-4
  16. Zhang LF, Moritani M, Honma S, Yoshida A, Shigenaga Y. Quantitative ultrastructure of slowly adapting lingual afferent terminals in the principal and oral nuclei in the cat. Synapse. 2001;41(2):96-111. https://doi.org/10.1002/syn.1064
  17. Bae YC, Kim JP, Choi BJ, Park KP, Choi MK, Moritani M, Yoshida A, Shigenaga Y. Synaptic organization of tooth pulp afferent terminals in the rat trigeminal sensory nuclei. J Comp Neurol. 2003;463:13-24. https://doi.org/10.1002/cne.10741
  18. 남혜경, 최갑식, 박국필, 배용철. 삼차신경주감각핵에서 치수유래 들신경섬유 종말의 정량적 분석. 대한해부학회지. 2002;35(5):439-452.
  19. Conradi S. Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface of the spinal cord of the adult cat. Acta Physiol Scand suppl. 1969;332:5-48.
  20. Bae YC, Ihn HJ, Park MJ, Ottersen OP, Moritani M, Yoshida A, Shigenaga Y. Identification of signal substances in synapses made between primary afferents and their associated axon terminals in the rat trigeminal sensory nuclei. J Comp Neurol. 2000;418:299-309. https://doi.org/10.1002/(SICI)1096-9861(20000313)418:3<299::AID-CNE5>3.0.CO;2-I
  21. Nakamura Y, Murakami T, Kikuchi M, Kubo Y, Ishimine S. Analysis of the circuitry responsible for primary afferent depolarization in the trigeminal spinal nucleus caudalis of cats. Exp Brain Res. 1977;29(3-4):405-418.
  22. Lovick TA. Primary afferent depolarization of tooth pulp afferents by stimulation in nucleus raphe magnus and the adjacent reticular formation in the cat: effects of bicuculline. Neurosci Lett. 1981;25(2):173-178. https://doi.org/10.1016/0304-3940(81)90327-X
  23. Lovick TA. The role of 5-HT, GABA and opioid peptides in presynaptic inhibition of tooth pulp input from the medial brainstem. Brain Res. 1983;289(1-2):135-142. https://doi.org/10.1016/0006-8993(83)90014-8
  24. Gmelin G, Zimmermann M. Effects of gamma-aminobutyrate and bicuculline on primary afferent depolarization of cutaneous fibres in the cat spinal cord. Neurosci. 1983;10(3):869-874. https://doi.org/10.1016/0306-4522(83)90224-5
  25. Shyu BC, Leung GM, Hu JW, Sessle BJ. Tooth pulp deafferentation is not associated with changes in primary afferent depolarization of facial afferent endings in the brain stem. Exp Neurol. 1993;123(2):243-250. https://doi.org/10.1006/exnr.1993.1157
  26. Burton H, Craig AD Jr. Distribution of trigeminothalamic projection cells in cat and monkey. Brain Res. 1979;161(3):515-521. https://doi.org/10.1016/0006-8993(79)90680-2
  27. Fukushima T, Kerr FW. Organization of trigeminothalamic tracts and other thalamic afferent systems of the brainstem in the rat: presence of gelatinosa neurons with thalamic connections. J Comp Neurol. 1979;183(1):169-184. https://doi.org/10.1002/cne.901830112
  28. Shigenaga Y, Nakatani Z, Nishimori T, Suemune S, Kuroda R, Matano S. The cells of origin of cat trigeminothalamic projections: especially in the caudal medulla. Brain Res. 1983;277(2):201-222. https://doi.org/10.1016/0006-8993(83)90928-9
  29. Zhang JD, Yang XL. Projections from subnucleus oralis of the spinal trigeminal nucleus to contralateral thalamus via the relay of juxtatrigeminal nucleus and dorsomedial part of the principal sensory trigeminal nucleus in the rat. J Hirnforsch. 1999;39(3):301-310.
  30. Yoshida A, Chen K, Moritani M, Yabuta NH, Nagase Y, Takemura M, Shigenaga Y. Organization of the descending projections from the parabrachial nucleus to the trigeminal sensory nuclear complex and spinal dorsal horn in the rat. J Comp Neurol. 1997;383(1):94-111. https://doi.org/10.1002/(SICI)1096-9861(19970623)383:1<94::AID-CNE8>3.0.CO;2-G
  31. Allen GV, Barbrick B, Esser MJ. Trigeminal-parabrachial connections: possible pathway for nociception-induced cardiovascular reflex responses. Brain Res. 1996;715(1-2):125-135. https://doi.org/10.1016/0006-8993(95)01580-9
  32. Zhang J, Luo P, Pendlebury WW. Light and electron microscopic observations of a direct projection from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat. Brain Res. 2001;917(1):67-80. https://doi.org/10.1016/S0006-8993(01)02911-0
  33. Bukowska D. Trigeminocerebellar projection to the paramedian lobule with emphasis on the climbing fibre zones: a retrograde tracing study in the rabbit. J Hirnforsch. 1996;37(2):159-172.
  34. Ikeda M, Matsushita M. Trigeminocerebellar projections to the posterior lobe in the cat, as studied by anterograde transport of wheat germ agglutinin-horseradish peroxidase. J Comp Neurol. 1992;316(2):221-237. https://doi.org/10.1002/cne.903160207
  35. Malick A, Burstein R. Cells of origin of the trigeminohypothalamic tract in the rat. J Comp Neurol. 1998;400(1):125-144. https://doi.org/10.1002/(SICI)1096-9861(19981012)400:1<125::AID-CNE9>3.0.CO;2-B