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Development of the Central Nervous System in Vertebrates pp 167–178Cite as

Two Phases of Pattern Formation in the Developing Rodent Trigeminal System

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Part of the book series: NATO ASI Series ((NSSA,volume 234))

Abstract

The patterning of neural connections, as reflected by the ordered projections between functionally related groups of cells, is a hallmark of the vertebrate CNS. The precision and specificity of such organization is especially striking in the interconnections within sensory systems wherein topographic representations of the periphery are mapped onto multiple central cell groups. These features are epitomized in the rodent trigeminal system: the array of vibrissae and sinus hairs on the snout is replicated in the punctate arrangement of cells and axons along the entire trigeminal neuraxis (see Woolsey, 1989 for a review). The question of how such ordered patterns come about has been addressed at various levels, including the establishment of regional specificity (Schneider, 1973), the acquisition of positional identity (rev., Gaze, 1970; Jacobson, 1978; Lund 1978), the selection of postsynaptic partners (Purves and Lichtman,1985), and so on. In this chapter we review our studies on pattern formation in the trigeminal system within the context of two particular aspects of this issue: the conferring of axial orientation of the somatotopic map in the CNS and the emergence of modular patterning within this map.

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References

  • Aitken, A.R. and Törk, I., 1988, Early development of serotonin-containing neurons and pathways as seen in wholemount preparations of the fetal rat brain, J. Comp. Neurol., 274:32.

    Article  PubMed  CAS  Google Scholar 

  • Altman, J. and Bayer, S.A., 1980a, Development of the brainstem in the rat: thymidine radiographic study of the time of origin of neurons of the lower medulla. J. Comp. Neurol., 194:1.

    Article  PubMed  CAS  Google Scholar 

  • Altman, J. and Bayer, S.A., 1980b, Development of the brainstem in the rat: thymidine radiographic study of the time of origin of neurons of the upper medulla, excluding the vestibular and auditory nuclei. J. Comp. Neurol., 194:37.

    Article  PubMed  CAS  Google Scholar 

  • Altman, J. and Bayer, S.A., 1980c, Development of the brainstem in the rat: thymidine radiographic study of the time of origin of neurons in the pontine region. J. Comp. Neurol., 194:905.

    Article  PubMed  CAS  Google Scholar 

  • Altman, J. and Bayer, S.A., 1982, Development of the cranial nerve ganglia and related nuclei in the rat. Adv. Anat. Embryol. Cell Biol., 74:1.

    Article  PubMed  CAS  Google Scholar 

  • Ard, M.D. and Bunge, R.P., 1988, Heparan sulfate proteoglycan and laminin immunoreactivity on cultured astrocytes: relationship to differentiation and neurite growth. J. Neurosci., 8:2844.

    PubMed  CAS  Google Scholar 

  • Bartsch, S., Bartsch, U., Dörries, U., Faissner, A., Weller, A., Ekblom, P. and Schachner, M., 1992, Expression of tenascin in the developing and adult cerebellar cortex. J. Neurosci., 12:736.

    PubMed  CAS  Google Scholar 

  • Bates, C.A. and Killackey, H.P., 1985, The organization of the neonatal rat’s brainstem trigeminal complex and its role in the formation of central trigeminal patterns. J. Comp. Neurol., 240:265.

    Article  PubMed  CAS  Google Scholar 

  • Belford, G.R. and Killackey, H.P., 1979, Vibrissae representation in subcortical trigeminal centers of the neonatal rat. J. Comp. Neurol., 183:305.

    Article  PubMed  CAS  Google Scholar 

  • Belford, G.R. and Killackey, H.P., 1980, The sensitive period in the development of the trigeminal system of the neonatal rat. J. Comp. Neurol., 193:335.

    Article  PubMed  CAS  Google Scholar 

  • Bernardo, K.L. and Woolsey, T.A., 1987, Axonal trajectories between mouse somatosensory thalamus and cortex. J. Comp. Neurol., 258:542.

    Article  PubMed  CAS  Google Scholar 

  • Blakemore, C. and Molnár, Z., 1990, Factors involved in the establishment of specific interconnections between thalamus and cerebral cortex . Cold Spring Harb. Symp. Quant. Biol., 55:491.

    Article  PubMed  CAS  Google Scholar 

  • Blue, M.E., Erzurumlu, R.S. and Jhaveri, S., 1991, A comparison of pattern formation by thalamocortical and serotonergic afferents in the rat barrel field cortex. Cerebral Cortex 1:380.

    Article  PubMed  CAS  Google Scholar 

  • Bunt, S.M. and Horder, T.J., 1983, Evidence for an orderly arrangement of optic axons within the optic nerves of the major mammalian vertebrate classes. J. Comp. Neurol., 213:94.

    Article  PubMed  CAS  Google Scholar 

  • Catalano, S.M., Robertson, R.T. and Killackey, H.P., 1991, Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat. Proc. Natl. Acad. Sci. U.S.A., 88:2999.

    Article  PubMed  CAS  Google Scholar 

  • Chiquet, M., 1989, Tenascin/Jl/cytotactin: the potential function of hexabrachion proteins in neural development. Dev. Neurosci., 11:266.

    Article  PubMed  CAS  Google Scholar 

  • Chuong, C.-M., Crossin, K.L. and Edelman, G.M., 1987, Sequential expression and different functions of multiple adhesion molecules during the formation of cerebellar cortical layers. J. Cell Biol., 104:331.

    Article  PubMed  CAS  Google Scholar 

  • Cooper, N.G.F. and Steindler, D.A., 1986a, Lectins demarcate the barrel subfield in the somatosensory cortex of the early postnatal mouse. J. Comp. Neurol. 249:157.

    Article  PubMed  CAS  Google Scholar 

  • Cooper, N.G.F. and Steindler, D.A., 1986b, Monoclonal antibody to glial fibrillary protein reveals a parcellation of individual barrels in the early postnatal mouse somatosensory cortex. Brain Res., 489:167.

    Article  Google Scholar 

  • Crossin, K. L., Hoffman, S., Tan, S.-S and Edelman, G.M., 1989, Cytotactin and its proteoglycan mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse. Dev. Biol., 136:381.

    Article  PubMed  CAS  Google Scholar 

  • Davies, A.M. and Lumsden, A.G.S., 1986, Fasciculation in the early mouse trigeminal nerve is not ordered in relation to the emerging pattern of whisker follicles. J. Comp. Neurol., 253:13.

    Article  PubMed  CAS  Google Scholar 

  • Durham, D. and Woolsey, T.A., 1984, Effects of neonatal whisker lesions on mouse central trigeminal pathways. J. Comp Neurol., 223:424.

    Article  PubMed  CAS  Google Scholar 

  • English, K.B., Burgess, P.R. and Kavka-Van Norman, D., 1980, Development of rat Merkel cells. J. Comp. Neurol., 194:475.

    Article  PubMed  CAS  Google Scholar 

  • Erzurumlu, R.S. and Jhaveri, S., 1990, Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex. Dev. Brain Res.. 56:229.

    Article  CAS  Google Scholar 

  • Erzurumlu, R.S. and Jhaveri, S., 1992a, Trigeminal ganglion cell processes are spatially ordered prior to the differentiation of the vibrissa pad. J. Neurosci., in press.

    Google Scholar 

  • Erzurumlu, R.S. and Jhaveri, S., 1992b, Emergence of connectivity in the embryonic rat parietal cortex. Cerebral Cortex, in press.

    Google Scholar 

  • Erzurumlu, R.S. and Killackey, H.P., 1983, Development of order in the rat trigeminal system . J. Comp. Neurol., 213:365.

    Article  PubMed  CAS  Google Scholar 

  • Erzurumlu, R.S., Bates, C.A. and Killackey, H.P., 1980, Differential organization of thalamic projection cells in the brainstem trigeminal complex of the rat. Brain Res., 198:427.

    Article  PubMed  CAS  Google Scholar 

  • Ferraro, A. and Barrera, S.E., 1936, Lamination of the medial lemniscus in Macaca rhesus. J. Comp. Neurol., 64:313.

    Article  Google Scholar 

  • Forbes, D.J. and Welt, C, 1981, Neurogenesis in the trigeminal ganglion of the albino rat: A quantitative autoradiographic study. J. Comp. Neurol., 199:133.

    Article  PubMed  CAS  Google Scholar 

  • Gaze, R.M., 1970, “The Formation of Nerve Connections”, Academic Press, NY.

    Google Scholar 

  • Harris, W.A., 1989, Local positional cues in the neuroepithelium guide retinal axons in embryonic Xenopus brains. Nature. 339:218.

    Article  PubMed  CAS  Google Scholar 

  • Halfter, W., Chiquet-Ehrismann, R. and Tucker, R.P., 1989, The effect of tenascin and embryonic basal lamina on the behavior and morphology of neural crest cells in vitro. Dev. Biol., 132:14.

    Article  PubMed  CAS  Google Scholar 

  • Horder, T.J. and Martin, K.A.C., 1978, Morphogenetics as an alternative to chemospecificity in the formation of nerve connections. in, “Cell-cell recognition”, v.32, Society for Exp. Biol. Symp., A.S.G. Curtis, ed., Cambridge Univ. Press, Cambridge. pp. 275.

    Google Scholar 

  • Horton, J.C., Greenwood, M.M. and Hubel, D.H., 1979, Non-retinotopic arrangement of fibers in the cat optic nerve. Nature, 282:720.

    Article  PubMed  CAS  Google Scholar 

  • Ivy, G.O. and Killackey, H.P, 1982, Ephemeral cellular segmentation in the thalamus of the neonatal rat. Dev. Brain Res.. 2:1.

    Article  Google Scholar 

  • Jacobson, M., 1978, “Developmental Neurobiology”, Second Edition, Plenum Press, NY.

    Google Scholar 

  • Jeanmonod, D., Rice, F.L and Van der Loos, H., 1981, Mouse somatosensory cortex: alterations in the barrel field following receptor injury at different postnatal ages. Neuroscience. 6:1503.

    Article  PubMed  CAS  Google Scholar 

  • Jensen, K.F. and Killackey, H.P, 1987, Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. J. Neurosci., 7:3529.

    PubMed  CAS  Google Scholar 

  • Jhaveri, S., 1973, “Altered retinal connections following partial tectal lesions in neonate hamsters.” M.S. Thesis, M.I.T., Cambridge, MA.

    Google Scholar 

  • Jhaveri, S., Erzurumlu, R.S. and Crossin, K., 1991, Barrel construction in rodent neocortex: Role of thalamic afferents versus extracellular matrix molecules. Proc. Natl. Acad. Sci. U.S.A, 88:4489.

    Article  PubMed  CAS  Google Scholar 

  • Killackey, H.P., 1985, Intrinsic order in the developing rat trigeminal system, in: “Development, Organization, and Processing in Somatosensory Pathways,” M. Rowe and W.D. Willis, eds., Liss, New York. pp. 43.

    Google Scholar 

  • Killackey, H.P. and Belford, G.R., 1979, The formation of afferent patterns in the somatosensory cortex of the neonatal rat. J. Comp. Neurol., 183:285.

    Article  PubMed  CAS  Google Scholar 

  • Killackey, H.P. and Shinder, A., 1981, Central correlates of peripheral pattern alterations in the trigeminal system of the rat. II. The effect of nerve section. Dev. Brain Res.. 1:121.

    Article  Google Scholar 

  • Kristt, D.A. and Walclman, J.B., 1982, Developmental organization of acetylcholinesterase-rich inputs to somatosensory cortex of the mouse. Anat. Embryol., 164:331.

    Article  PubMed  CAS  Google Scholar 

  • Krystosek, A. and Seeds, N.W., 1981, Plasminogen activator release at the neuronal growth cone. Science. 213:1532.

    Article  PubMed  CAS  Google Scholar 

  • Lidov, H.G.W. and Molliver, M.E., 1982, An immunohistochemical study of serotonin development in the rat: ascending pathways and terminal fields. Brain Res. Bull.. 8:389.

    Article  PubMed  CAS  Google Scholar 

  • Lochter, A., Vaughan, L., Kaplony, A., Prochiantz, A., Schachner, M. and Faissner, A., 1991, Jl/Tenascin in substrate-bound and soluble form displays contrary effects on neurite outgrowth. J. Cell Biol., 113:1159.

    Article  PubMed  CAS  Google Scholar 

  • Lund, R.D., 1978, “Development and Plasticity of the Brain: An Introduction”, Oxford Univ. Press, NY.

    Google Scholar 

  • Ma, P.K.M. and Woolsey, T.A., 1984, Cytoarchitectonic correlates of the vibrissae in the medullary trigeminal complex of the mouse. Brain Res.. 306:374.

    Article  PubMed  CAS  Google Scholar 

  • Molnár, Z. and Blakemore, C., 1990, Relationship of corticofugal and corticopetal projections in the prenatal establishment of projections from thalamic nuclei to specific cortical areas of the rat. Proc. Physiol. Soc. (Lond.), 104P.

    Google Scholar 

  • Pittman, R.N., Ivins, J.K. and Buettner, H.M., 1989, Neuronal plasminogen activators: cell surface binding sites and involvement in neurite outgrowth. J.Neurosci., 9:4269.

    PubMed  CAS  Google Scholar 

  • Purves, D. and Lichtman, J.W., 1985, “Principles of Neural Development”, Sinauer Assoc. Press, Sunderland, MA.

    Google Scholar 

  • Nelson, S.B. and LeVay, S., 1985, Topographic organization of the optic radiation of the cat. J. Comp. Neurol., 240:322.

    Article  PubMed  CAS  Google Scholar 

  • Rager, G.H., 1980, Development of the retinotectal projection in the chicken. Adv. Anat. Embryol. Cell Biol., 63:1.

    Article  Google Scholar 

  • Reese, B.E. and Cowey, A., 1990, Fiber organization of the monkey’s optic tract: I. Segregation of functionally distinct optic axons. J.Comp. Neurol., 295:385.

    Article  PubMed  CAS  Google Scholar 

  • Rhoades, R.W., Chiaia, N.L. and MacDonald, G.J., 1990a, Topographic organization of the peripheral projections of the trigeminal ganglion in the fetal rat. Somatosens. Mot. Res., 7:67.

    Article  PubMed  CAS  Google Scholar 

  • Rhoades, R.W., Bennett-Clark, C.A., Chiaia, N.L., White, F.A., MacDonald, G.J., Haring, J.H. and Jacquin, M.F., 1990b, Development and lesion-induced reorganization of the cortical representation of the rat’s body surface as revealed by immunocytochemistry for serotonin. J. Comp. Neurol., 293:190.

    Article  PubMed  CAS  Google Scholar 

  • Rhoades, R.W., Enfiejian, H.L., Chiaia, N.L., MacDonald, G.J., Miller, M.W., McCann, P. and Goddard, C.M., 1991, Birthdates of trigeminal ganglion cells contributing axons to the infraorbital nerve and specific vibrissal follicles in the rat. J. Comp. Neurol., 307:163.

    Article  PubMed  CAS  Google Scholar 

  • Rice, F.L. and Van der Loos, H., 1977, Development of the barrels and barrel field in the somatosensory cortex of the mouse. J. Comp. Neurol., 171:545.

    Article  PubMed  CAS  Google Scholar 

  • Rice, F.L., Gomez, C., Barstow, C., Burnet, A. and Sands, P., 1985, A comparative analysis of the development of the primary somatosensory cortex: interspecies similarities during barrel and lamina development. J. Comp. Neurol., 236:477.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, R.T., 1987, A morphogenic role for transiently expressed acetylcholinesterase in developing thalamocortical systems? Neurosci. Lett., 75:259.

    Article  PubMed  CAS  Google Scholar 

  • Rusoff, A.C., 1984, Paths of axons in the visual system of perciform fish and implications of these paths for rules governing axonal growth. J. Neurosci., 4:1414.

    PubMed  CAS  Google Scholar 

  • Schlaggar, B.L. and O’Leary, D.D.M, 1991, A periphery-related pattern is evident in rat somatosensory cortex at birth. Soc. Neurosci. Abstr., 17:1126.

    Google Scholar 

  • Schneider, G.E., 1973, Early lesions of the superior colliculus: Factors affecting the formation of abnormal retinal projections. Brain. Behav. Evol., 8:93.

    Google Scholar 

  • Schlumpf, M., Shoemaker, W.J. and Bloom, F.E., 1980, Innervation of embryonic rat cerebral cortex by catecholamine-containing fibers. J. Comp. Neurol., 192:361.

    Article  PubMed  CAS  Google Scholar 

  • Silver, J. and Sidman, R.L., 1980, A mechanism for the guidance and topographic patterning of retinal ganglion cell axons. J. Comp. Neurol., 189:101.

    Article  PubMed  CAS  Google Scholar 

  • Stainier, D.Y.R. and Gilbert, W., 1991, Pioneer neurons in the mouse trigeminal sensory system. Proc. Natl. Acad. Sci. USA 87:923.

    Article  Google Scholar 

  • Steindler, D.A., Cooper, N.G.F., Faissner, A. and Schachner, M., 1989, Boundaries defined by adhesion molecules during development of the cerebral cortex: the Jl/tenascin glycoprotein in the mouse somatosensory barrel cortical field. Dev. Biol., 131:243.

    Article  PubMed  CAS  Google Scholar 

  • Torrealba, F., Guillery, R.W., Eysel, U., Polley, E.H. and Mason, C.A., 1982, Studies of retinal representations within the cat’s optic tract. J. Comp. Neurol., 211:377.

    Article  PubMed  CAS  Google Scholar 

  • Van der Loos, H., 1976, Barreloids in mouse somatosensory thalamus. Neurosci. Lett., 2:1.

    Article  Google Scholar 

  • Van der Loos, H. and Welker, E., 1985, Development and plasticity of somatosensory brain maps, in: “Development, Organization and Processing in Somatosensory Pathways,” M. Rowe and W.D. Willis, eds., Liss, New York.

    Google Scholar 

  • Van der Loos, H. and Woolsey, T.A., 1973, Somatosensory cortex: structural alterations following early injury to sense organs. Science. 179:395.

    Article  PubMed  Google Scholar 

  • Van Exan, R.J. and Hardy, M.H., 1980, A spatial relationship between innervation and the early differentiation of vibrissa follicles in the embryonic mouse. J. Anat., 131:643.

    PubMed  Google Scholar 

  • Verney, C., Berger, B., Baulac, M., Helle, K.B. and Alvarez, C., 1984, Dopamine-β-Hydroxylase-like immunoreactivity in the fetal cerebral cortex of the rat: Noradrenergic ascending pathways and terminal fields. Int. J. Dev. Neurosci., 2:491.

    Article  CAS  Google Scholar 

  • Walker, A.E., 1937, Experimental anatomical studies of the topical localization within the thalamus of the chimpanzee. Proc. Kon. Ned. Akad. Wet., 40:198.

    Google Scholar 

  • Walker, A.E. and Weaver, T.A., 1942, The topical organization and termination of the fibers of the posterior columns in Macaca mulatta. J. Comp. Neurol., 76:145.

    Article  Google Scholar 

  • Wallace, J.A. and Lauder, J.M., 1983, Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res. Bull.. 10:459.

    Article  PubMed  CAS  Google Scholar 

  • Walsh, C. and Guillery, R.W., 1985, Age-related fiber order in the optic tract of the ferret. J. Neurosci., 5:3061.

    PubMed  CAS  Google Scholar 

  • Walsh, C., Polley, E.H., Hickey, T.L. and Guillery, R.W., 1983, Generation of cat retinal ganglion cells in relation to central pathways. Nature, 302:611.

    Article  PubMed  CAS  Google Scholar 

  • Wehrle, B. and Chiquet, M., 1990, Tenascin is accumulated along developing peripheral nerves and allows neurite outgrowth in vitro. Development. 110:401.

    PubMed  CAS  Google Scholar 

  • Welker, E. and Van der Loos, H., 1986, Quantitative correlation between barrelfield size and the sensory innervation of the whiskerpad: a comparative study in six strains of mice bred for different patterns of mystacial vibrissae. J. Neurosci., 6:3355.

    PubMed  CAS  Google Scholar 

  • Williams R.W. and Rakic, P., 1985, Dispersion of growing axons within the optic nerve of the embryonic monkey. Proc. Natl. Acad. Sci. USA., 82:3906.

    Article  PubMed  CAS  Google Scholar 

  • Woolsey, T.A., 1989, Peripheral alterations and somatosensory development, in “Development of Sensory Systems in Mammals”, J.R. Coleman, ed., John Wiley, NY. pp 462.

    Google Scholar 

  • Woolsey, T.A. and Van der Loos, H., 1970, The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. Brain Res., 17:205.

    Article  PubMed  CAS  Google Scholar 

  • Yamakado, M and Yohro, T., 1979, Subdivision of mouse vibrissae on an embryological basis, with descriptions of variations in the number and arrangement of sinus hairs and cortical barrels in BALB/c (nu/+; nude, nu/nu) and hairless (hr/hr) strains. Am. J. Anat., 155:153.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambribge, MA, 02139, USA

    Sonal Jhaveri & Reha Erzurumlu

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  1. Sonal Jhaveri
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  1. New York Medical College, Valhalla, New York, USA

    S. C. Sharma

  2. Université Notre Dame de la Paix, Namur, Belgium

    A. M. Goffinet

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Jhaveri, S., Erzurumlu, R. (1992). Two Phases of Pattern Formation in the Developing Rodent Trigeminal System. In: Sharma, S.C., Goffinet, A.M. (eds) Development of the Central Nervous System in Vertebrates. NATO ASI Series, vol 234. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3018-3_12

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