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Morphological and neurochemical plasticity of rat mesencephalic trigeminal neurons

Angel Dandov, Dimitrinka Atanasova, Nikolai Lazarov

Abstract

The mesencephalic trigeminal nucleus (Me5) is a unique structure in the central nervous system (CNS), made up of pseudounipolar sensory neurons. It is also a suitable paradigm for studying the plastic alterations in neurons. It is known that the Me5 neurons utilize various neurotransmitters under normal conditions, though little information is available about the morphological and chemical events taking place in the nucleus after injury. This review provides concise description of the structural adaptive changes in Me5 neurons following peripheral axotomy of the masseteric nerve. Furthermore, it validates NADPH-diaphorase activity in them, and using immunohistochemistry for glutamate (Glu), substance P (SP), calcitonin-gene related protein (CGRP), neuropeptide tyrosine (NPY) and galanin (GAL), it deals with the altered neurochemical phenotype of the injured neurons. Our results distinctly show that the Me5 neurons in the rat are extremely sensitive to peripheral injury and we demonstrate their distinct structural and neurochemical plasticity. The adaptive morphological alterations comprise of both qualitative and quantitative
alterations in the axotomized Me5 population which are statistically significant when compared with the number and phenotype of the neurons on the contralateral intact side. Besides, the axotomy-induced alterations in the neurochemical character of Me5 are best signified by the down-regulation of the classical neurotransmitters under normal conditions, and the up-regulation of
nitric oxide synthase and de novo synthesis of certain neuroactive substances such as NPY, SP, GAL and VIP. It can be inferred that the described phenomena only occur in the nucleus in cases of injury and changes in the environmental cues, and serve as adaptive mechanisms and powerful trophic factors for the neuronal survival in the Me5. There is, undoubtedly, still a long way to go in order to clarify the dynamic and plastic alterations occurring in the CNS in health and disease, and also explain their role in such important functions as pain, perception, learning, cognition and memory.


Keywords

axotomy, mesencephalic trigeminal neurons, neurotransmitters, plasticity, rat

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References

Cajal S. Beitrag zum Studium der Medulla Oblongata, des Kleinhirns und des Ursprungs der Gehirnnerven. Johann Ambrosius Barh, Leipzig, 1896. DOI:10.5962/bhl.title.61878

Cajal S. Histologie du Système Nerveaux de l’Homme et des Vertèbrès, vol. 1 A. Maloine, Paris, 1909. DOI:10.5962/bhl.title.48637

Scharf JH. Sensible Ganglien. In: Möllendorff M, Barg-mann W, editors. Handbuch der mikroskopischen Anatomie des Menschen Bd. 4/3, Springer-Verlag, Berlin, 1958; 290–300.

Brodal A. Neurological Anatomy in Relation to Clinical Medicine, 3rd ed., Oxford University Press, New York, 1981. ISBN-13: 978-0195026948

Usunoff KG, Marani E, Schoen JH. The trigeminal system in man. Adv Anat Embryol Cell Biol 1997; 136: 1-126. DOI:10.1007/978-3-642-60779-0

Marani E, Usunoff KG. The trigeminal motonucleus in man. Arch Physiol Biochem 1998; 106: 346-354. DOI:10.1076/apab.106.5.346.4364

Lazarov NE. The mesencephalic trigeminal nucleus in the cat, Adv Anat Embryol Cell Biol 2000; 153: 1-103. DOI:10.1007/978-3-642-57176-3

Darian-Smith I. The trigeminal system. In: Iggo A, editor. Handbook of Sensory Physiology, Somatosensory System, Springer, Berlin, 1973; 271-314. DOI:10.1007/978-3-642-65438-1_10

Johnston JB. The radix mesencephalica trigemini. J Comp Neurol 1909; 19: 593-644. DOI:10.1002/cne.920190602

Freeman W. The relationship of the radix mesencephalica trigemini to the extraocular muscles. Arch Neurol Psychiatry 1925; 14: 111-113.

Dubner R, Sessle B, Storey A. The Neural Basis of Oral and Facial Function, Plenum Press, London, 1978. DOI:10.1016/0002-9416(79)90109-X

Davies AM. The trigeminal system: an advantageous experimental model for studying neuronal development. Development 1988; 103: 175-183.

Shigenaga Y, Sera M, Nishimori T, Suemune S, Ni-shimura M, Yoshida A, Tsuru K. The central projec-tions of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord. J Comp Neurol 1988; 268: 489-507. DOI:10.1002/cne.902680403

Kruger L, Young RF. Specialised features of the trigeminal nerve and its central connections. In: Samii M, Janeta PJ, editors. The Cranial Nerves. Springer, Berlin, 1981; 273-301. DOI:10.1007/978-3-642-67980-3_37

Pfaller K, Arvidsson J. Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. J Comp Neurol 1988; 268: 91-108. DOI:10.1002/cne.902680110

Yoshida A, Yasuda K, Dostrovsky JO, Bae YC, Take-mura M, Shigenaga Y, Sessle BJ. Two major types of premotoneurons in the feline trigeminal nucleus oralis as demonstrated by intracellular staining with horseradish peroxidase. J Comp Neurol 1994; 347: 495-514. DOI:10.1002/cne.903470403

Yoshida S, Oka H. Membrane properties of dissociated trigeminal mesencephalic neurons of the adult rat. Neurosci Res 1998; 30: 227-234. DOI:10.1016/s0168-0102(98)00003-0

Alvarado-Mallart MR, Batini C, Buisseret-Delmas C, Corvisier J. Trigeminal representations of the masticatory and extraocular proprioceptors as revealed by horseradish peroxidase retrograde transport. Exp Brain Res 1975; 23:167-179. DOI:10.1007/bf00235459

Capra NF, Anderson KV, Atkinson RC. Localization and morphometric analysis of masticatory muscle afferent neurons in the nucleus of the mesencephalic root of the trigeminal nerve in the cat. Acta Anat (Basel) 1985; 122:115-125. DOI:10.1159/000145992

Shigenaga Y, Yoshida A, Mitsuhiro Y, 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; 461: 143-149. DOI:10.1016/0006-8993(88)90732-9

Jerge CR. Organization and function of the trigeminal mensencephalic nucleus. J Neurophysiol 1963; 26: 379-392. DOI:10.1152/jn.1963.26.3.379

Byers MR, Holland GR. Trigeminal nerve endings in gingiva, junctional epithelium and periodontal ligament of rat molars, as demonstrated by autoradiography. Anat Rec 1977; 188: 509-523. DOI:10.1002/ar.1091880409

Byers MR. Sensory innervation of periodontal ligament of rat molars consists of unencapsulated Ruffini-like mechanoreceptors and free nerve endings. J Comp Neurol 1985; 231: 500-518. DOI:10.1002/cne.902310408

Byers MR, O’Connor TA, Martin RF, Dong WK. Mesencephalic trigeminal sensory neurons of cat: axon pathways and structure of mechanoreceptive endings in periodontal ligament. J Comp Neurol 1986; 250: 181-191. DOI:10.1002/cne.902500205

Shigenaga Y, Yoshida A, Mitsuhiro Y, Doe K, Suemune S. Morphology of single mesencephalic trigeminal neurons innervating periodontal ligament of the cat. Brain Res 1988; 448: 331-338. DOI:10.1016/0006-8993(88)91272-3

Byers MR, Dong WK. Comparison of trigeminal receptor location and structure in the periodontal ligament of different types of teeth from the rat, cat, and monkey. J Comp Neurol 1989; 279: 117-127. DOI:10.1002/cne.902790110

Linden RWA, Millar BJ, Halata Z. A comparative physiological and morphological study of periodontal ligament mechanoreceptors represented in the trigeminal ganglion and the mesencephalic nucleus of the cat. Anat Embryol 1994; 190: 127-135. DOI:10.1007/BF00193410

Amano N, Yoshino K, Andoh S, Kawagishi S. Representation of tooth pulp in the mesencephalic trigeminal nucleus and the trigeminal ganglion in the cat, as revealed by retrogradely transported horseradish peroxidase. Neurosci Lett 1987; 82: 127-132. DOI:10.1016/0304-3940(87)90116-9

Yoshino K, Andoh S, Kawagishi S, Yamauchi M, Jones TE, Amano N. Innervation of the tooth pulp by the mes-encephalic trigeminal nucleus in the cat: a retrograde horseradish peroxidase study. Brain Res 1989; 503: 152-155. DOI:10.1016/0006-8993(89)91717-4

Byers MR, Matthews B. Autoradiographic demonstrations of ipsilateral and contralateral sensory nerve endings in cat dentin, pulp and periodontium. Anat Rec 1981; 201:249-260. DOI:10.1002/ar.1092010205

Costa M, Furness JB, Gibbins IL. Chemical coding of enteric neurons. Prog Brain Res 1986; 68: 217-239. DOI:10.1016/S0079-6123(08)60241-1

Hökfelt T, Zhang X, Wiesenfeld-Hallin Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 1994; 17: 22-30. DOI:10.1016/0166-2236(94)90031-0

Raappana P, Arvidsson J. The reaction of mesencephalic trigeminal neurons to peripheral nerve transection in the adult rat. Exp Brain Res 1992; 90: 567-571. DOI:10.1007/bf00230940

Ichikawa H, Jin HW, Terayama S, Yamaai T, Matsuo S, Sugimoto T. The reduction of proprioceptors in the mesencephalic trigeminal tract nucleus after neonatal masseteric nerve transection; effect of brain-derived neurotrophic factor. Brain Res 2007; 1153: 98-102. DOI:10.1016/j. brainres.2007.03.060

Lazarov NE. Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus. Prog Neurobiol 2002; 66:19-59. DOI:10.1016/s0301-0082(01)00021-1

Lazarov NE. Neurobiology of orofacial proprioception. Brain Res Rev 2007; 56: 362-383. DOI:10.1016/j.brain-resrev.2007.08.009

Navarro X, Vivó M, Valero-Cabré A. Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 2007; 82: 163-201. DOI:10.1016/j.pneurobio.2007.06.005

Allen WF. Application of the Marchi method to the study on the radix mesencephalica trigemini in the guinea pig. J Comp Neurol 1919; 30: 169-216. DOI:10.1002/cne.900300202

Corbin KB. Probst’s tract in the cat. J Comp Neurol 1940; 77: 455-467. DOI:10.1002/cne.900770302

Szentágothai J. Anatomical considerations of monosynaptic reflex arc. J Neurophysiol 1948; 11: 445-454. DOI:10.1152/jn.1948.11.5.445

Dault SH, Smith RD. A quantitative study of the nucleus of the mesencephalic tract of the trigeminal nerve of the cat. Anat Rec 1969; 165: 79-87. DOI:10.1002/ar.1091650109

Imamoto K. Electron microscopic observations in the trigeminal mesencephalic nucleus following neurotomy of the third division of the trigeminal nerve. Arch Histol Jpn 1972; 34: 361-374. DOI:10.1679/aohc1950.34.361

Aldskogius H, Arvidsson J. Nerve cell degeneration in the trigeminal ganglion of the adult rat following peripheral nerve transection. J Neurocytol 1978; 7: 229-250. DOI:10.1007/bf01217921

Lepousez G, Nissant A, Lledo PM. Adult neurogenesis and the future of the rejuvenating brain circuits. Neuron 2015; 86: 387-401. DOI:10.1016/j.neuron.2015.01.002

Umemoto S, Noguchi K, Kawai Y, Senba E. The expression of neuropeptides and their mRNAs in the trigemi-nal mesencephalic nucleus following masseteric nerve transection. Brain Res Mol Brain Res 1994; 23: 93-99. DOI:10.1016/0169-328x(94)90215-1

Yoshida A, Ichikawa H, Sugimoto T. CGRP in peripherally axotomized mesencephalic trigeminal neurones of the rat. Neuroreport 1995; 6: 837-840. DOI:10.1097/00001756-199504190-00003

Lazarov N, Dandov A, Stoyanova I, Chouchkov C. Axotomy-induced alterations in the neurochemical content of cat mesencephalic trigeminal nucleus neurons. It J Anat Embryol [Suppl] 1999; 104: 386.

Lazarov N, Dandov A. Ultrastructural patterns of glutamate and GABA immunolabelling in the cat mesencephalic trigeminal nucleus. C R Acad Bulg Sci 2000; 53:109-112.

Dandov AD, Atanasova DY, Lazarov NE. Morphological changes in the rat mesencephalic trigeminal nucleus following peripheral axotomy. C R Acad Bulg Sci 2016; 69(6): 801-806.

Lipton SA, Kater SB. Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci 1989; 12: 265-270. DOI:10.1016/0166-2236(89)90026-x

Copray JCVM, Liem RSB. Survival and neurite formation of mesencephalic trigeminal neurones of the rat in vitro. Arch Oral Biol 1993; 38: 547-557. DOI:10.1016/0003-9969(93)90119-7

Arvidsson J, Rappaana P, Diez M, Hökfelt T. Expression of neuropeptides in the rat mesencephalic trigeminal nucleus after peripheral axotomy. Neuroreport 1994; 5: 1269-1272. DOI:10.1097/00001756-199406020-00029

Wakisaka S, Takikita S, Youn SH, Kurisu K. Partial co-existence of neuropeptide Y and calbindin D28k in the trigeminal ganglion following peripheral nerve axotomy of the inferior alveolar nerve in the rat. Brain Res 1996; 707: 228-234. DOI:10.1016/0006-8993(95)01262-1

Larsen JO, Hannibal J, Knudsen SM, Fahrenkrug J. Expression of pituitary adenylate cyclase-activating polypeptide (PACAP) in the mesencephalic trigeminal nucleus of the rat after transsection of the masseteric nerve. Mol Brain Res 1997; 46: 109-117. DOI:10.1016/s0169-328x(96)00279-3

De Gandarias JM, Mendez PL, Vegas L, Echevarría E, Maza JL, Casis L. Infraorbital nerve transection increases NADPH-diaphorase activity in the rat mesencephalic trigeminal nucleus. J Hirnforsch 1999; 39: 567-571.

Copray JCVM, Ter Horst GJ, Liem RSB, van Willigen JD. Neurotransmitters and neuropeptides within the mesencephalic trigeminal nucleus of the rat: an immunohistochemical analysis. Neuroscience 1990; 37: 399-411. DOI:10.1016/0306-4522(90)90410-6

Chandler SH. Evidence for excitatory amino acid trans-mission between mesencephalic nucleus of V afferents and jaw-closer motoneurons in the guinea pig. Brain Res 1989; 477: 252-264. DOI:10.1016/0006-8993(89)91413-3

Lazarov N, Dandov A. Distribution of NADPH-diapho-rase/nitric oxide synthase in the trigeminal ganglion and mesencephalic trigeminal nucleus of the cat. A histochemical and immunohistochemical study. Acta Anat 1998; 163:

- 200. DOI:10.1159/000046498

Stoyanova II, Lazarov NE. Localization of nitric oxide synthase in rat trigeminal primary afferent neurons using NADPH-diaphorase histochemistry. J Mol Histol 2005; 36: 187-193. DOI:10.1007/s10735-005-1694-3

Varathan V, Shigenaga Y, Takemura M. Nitric oxide synthase/nicotinamide adenine dinucleotide phosphate-diaphorase in the brainstem trigeminal nuclei after transection of the masseteric nerve in rats. J Neurosci Res 2001; 66: 428-438. DOI:10.1002/jnr.1235

Elcock C, Boissonade FM, Robinson PP. Changes in neuropeptide expression in the trigeminal ganglion following inferior alveolar nerve section in the ferret. Neuroscience 2001; 102: 655-667. DOI:10.1016/s0306-4522(00)00508-x

Dandov A, Draganov M, Lazarov N. Synthesis of galanin and neuropeptide Y in the rat mesencephalic trigeminal nucleus after injury of n. massetericus. Trakia J Sci 2005; 3: 1-5.

Dandov A, Penkova Zh, Lazarov N. De novo expression of neuropeptides in the mesencephalic trigeminal nucleus of the rat after masseteric nerve injury. Acta Morhol Antropol 2010; 15: 27-30.

Noguchi K, De León M, Nahin RL, Senba E, Ruda MA. Quantification of axotomy-induced alteration of neuropeptide mRNAs in dorsal root ganglion neurons with special reference to neuropeptide Y mRNA and the effects of neonatal capsaicin treatment. J Neurosci Res 1993; 35:54-66. DOI:10.1002/jnr.490350108

Nielsch U, Keen P. Reciprocal regulation of tachykinin- and vasoactive intestinal peptide-gene expression in rat sensory neurones following cut and crush injury. Brain Res 1989; 481: 25-30. DOI:10.1016/0006-8993(89)90481-2

Jacobs JS, Miller MW. Expression of nerve growth factor, p75, and the high affinity neurotrophin receptors in the adult rat trigeminal system: evidence for multiple trophic support systems. J Neurocytol 1999; 28: 571-595. DOI:10.1023/a:1007019422675

Lazarov NE, Dandov A, Stoyanova I, Chouchkov CN. Calcium-binding proteins in the mesencephalic trigeminal nucleus of the cat. Arch Physiol Biochem 1998; 106: 370-377. DOI:10.1076/apab.106.5.370.4366

Honda CN. Differential distribution of calbindin-D28k and parvalbumin in somatic and visceral sensory neurons. Neuroscience 1995; 68: 883-892. DOI:10.1016/0306-4522(95)00180-q

Medici T, Shortland PJ. Effects of peripheral nerve injury on parvalbumin expression in adult rat dorsal root ganglion neurons. BMC Neurosci 2015; 16: 93. DOI:10.1186/s12868-015-0232-9

Blaustein MP. Calcium transport and buffering in neurons. Trends Neurosci 1988; 11: 438-443. DOI:10.1016/0166-2236(88)90195-6

Baimbridge KG, Miller JJ, Parkes CO. Calcium-binding protein distribution in the rat brain. Brain Res 1982; 239:

- 25. DOI:10.1016/0006-8993(82)90526-1

Celio MR. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 1990; 35: 375-475. DOI:10.1016/0306-4522(90)90091-h

Sasaki Y, Wakisaka S, Kurisu K. Effects of peripheral axotomy of the inferior alveolar nerve on the levels of neuropeptide Y in rat trigeminal primary afferent neu-rons. Brain Res 1994; 664: 108-114. DOI:10.1016/0006-8993(94)91960-7

Wakisaka S, Youn SH, Miyawaki Y, Kurisu K. The effects of peripheral nerve injury of the masseteric nerve on the levels of calcium binding proteins and neuropeptide Y, and their correlation in the mesencephalic trigeminal nucleus of the rat. Brain Res 1996; 735: 249-256. DOI:10.1016/0006-8993(96)00585-9




DOI: http://dx.doi.org/10.14748/bmr.v30.6388

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About The Authors

Angel Dandov
Medical University-Sofia
Bulgaria

Department of Anatomy and Histology

Dimitrinka Atanasova
Department of Anatomy, Faculty of Medicine, Trakia University, Stara Zagora
Bulgaria

Institute of Neurobiology, Bulgarian Academy of Sciences, Sofia

Nikolai Lazarov
Department of Anatomy and Histology, Medical University-Sofia
Bulgaria

Institute of Neurobiology, Bulgarian Academy of Sciences, Sofia

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