Abstract
The topographic patterns of peripheral receptors and effectors seem to contribute to the construction of the neuronal circuit in the central nervous system (CNS) in mammals. Many patterns replicating those of the periphery have been found in the CNS, and fasciculation has been regarded as having a central role in the pattern replication. The house shrew, Suncus murinus, is an excellent species in which to study this topic because it has a vibrissae system arranged in a single ordered fashion and extraordinarily well-developed trigeminal spinal tracts. Using immunostaining and retrograde-tracing techniques, we examined the developmental pattern of the maxillary nervous system in the house shrew. The results indicate that the basic pattern of axonal extension reiterates with a parallel arrangement throughout the course of development except at a site in the brainstem where the central processes bifurcate into ascending and descending branches. Dorsoventral inversion of the peripheral pattern in the spinal tract occurs with this dualleveled bifurcation in association with the mediolaterally ordered entry of the central processes into the brainstem. The basic pattern of the central processes is established prior to the appearance of the vibrissae, indicating that the basic topographic pattern of the maxillary nerve is not related to the vibrissae system. The fasciculation pattern does not correspond to the overall layout of the arrays of vibrissae, and there are frequent exchanges of axons between fascicles both in the periphery and centrally. The parallel organization of the majority of the processes, together with the free exchange of processes between fascicles, suggests that these processes have an important role in the formation of the fasciculation and somatotopic patterns.
Similar content being viewed by others
References
Arumäe U, Pirvola U, Palgi J, Kiema T, Palm K, Moshnyakov M, Ylikoski J, Saarma M (1993) Neurotrophins and their receptors in rat peripheral trigeminal system during maxillary nerve growth. J Cell Biol 122:1053–1065
Belford GR, Killackey HP (1979) Vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 183:305–322
Buchman VL, Davies AM (1993) Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. Development 118:989–1001
Covell DA, Noden DM (1989) Embryonic development of the chick primary trigeminal sensory-motor complex. J Comp Neurol 286:488–503
Davies AM (1988) The trigeminal system: an advantageous experimental model for studying neuronal development. Development 103:175–183
Davies AM (1994) Intrinsic programmes of growth and survival in developing vertebrate neurons. Trends Neurosci 17:195–199
Davies AM, Lumsden AGS (1986) Fasciculation in the early mouse trigeminal nerve is not ordered in relation to the emerging pattern of whisker follicles. J Comp Neurol 253:13–24
Davies AM, Bandtlow C, Heumann R, Korsching S, Rohrer H, Thoenen H (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326:353–358
Erzurumlu RS, Jhaveri S (1992) Trigeminal ganglion cell processes are spatially ordered prior to the differentiation of the vibrissae pad. J Neurosci 12:3946–3955
Erzurumlu RS, Killackey HP (1983) Development of order in the rat trigeminal system. J Comp Neurol 213:365–380
Heaton MB, Moody SA (1980) Early development and migration of the trigeminal motor nucleus in the chick embryo. J Comp Neurol 189:61–99
Ibáñez CF, Ernfors P, Timmusk T, Ip NY, Arenas E, Yancopoulos GD, Persson H (1993) Neurotrophin-4 is a target-derived neurotrophic factor for neurons of the trigeminal ganglion. Development 117:1345–1353
Kerr FWL (1963) The divisional organization of afferent fibers of the trigeminal nerve. Brain 86:721–732
Kruger L, Michel F (1962) A morphological and somatotopic analysis of single unit activity in the trigeminal sensory complex of the cat. Exp Neurol 5:139–156
Lumsden AGS, Davies AM (1986) Chemotropic effect of specific target epithelium in the developing mammalian nervous system. Nature 323:538–539
Nomura S, Uemura-Sumi M, Oda S (1989) Histochemical demonstration of cytochrome oxidase activity and infraorbital nerve afferents within the trigeminal sensory nuclei of house musk shrew, Suncus murinus. In: Kubota K (ed) Mechanobiological research on the masticatory system. VEB Verlage für Medizin and Biologie. Berlin, pp 87–92
Sundin OH, Eichele G (1990) A homeo domain protein reveals the metameric nature of the developing chick hindbrain. Genes Dev 4:1267–1276
Welker E, Van der Loos H (1986) Quantitative correlation between barrel-field size and the sensory innervation of the whisker pad: a comparative study in six strains of mice bred for different patterns of mystacial vibrissae. J Neurosci 6:3355–3373
Welker E, Soriano E, Van der Loos H (1989) Plasticity in the barrel cortex of the adult mouse: effects of peripheral deprivation on GAD-immunoreactivity. Exp Brain Res 74:441–452
Wyatt S, Davies AM (1993) Regulation of expression of mRNAs encoding the nerve growth factor receptors p75 and trkA in developing sensory neurons. Development 119:635–648
Yamakado M, 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 155:153–174
Yasui K (1992) Embryonic development of the house shrew (Suncus murinus) I. Embryos at stages 9 and 10 with 1 to 12 pairs of somites. Anat Embryol 186:49–65
Yasui K, Agata K, Tanaka S (1994) Neurofilament expression in lens cells of the house shrew, Suncus murinus. Anat Embryol 189:401–407
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Yasui, K., Arakaki, R., Uemura, M. et al. Developmental pattern of axonal pathways in the house shrew maxillary nerve. Anat Embryol 194, 205–213 (1996). https://doi.org/10.1007/BF00187131
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00187131