Summary
Onychophorans are ‘living fossils’ frequently purported to have evolved from the same ancestor as the arthropods and annelids. In the CNS ofPeripatus acacioi, beneath an outer acellular neural lamella, glial cells ensheath the cerebral ganglion and the nerve cords. These glial cells are, however, attenuated and rather few in number and, although they interdigitate with one another, they seem to lack intercellular junctions. Exogenous tracers penetrate between them and into the underlying neuropile, suggesting that there is no structural blood-brain barrier. Throughout the nervous tissue, extracellular spaces occur which contain banded collagen fibrils embedded in a matrix material. Thin glial cell processes, characterized by dense filaments, surround these regions and frequently form hemi-desmosomes with the extracellular matrix. The peripheral nerve cell bodies have a range of diameters; some have the characteristics of neurosecretory neurons. Granules in such neurons are produced by the Golgi saccules and associated fenestrated membranes which also possess many coated vesicles. Comparable granules are also found in axonal tracts, but no distinct peripheral neurohaemal areas have been found. Lysosomes are common in the nerve cell bodies and are frequently in the form of multivesicular bodies or large phagocytic vacuoles. Beneath the outer nerve cells lie many tracheae, arranged as a ring around the central neuropile which consists of glial processes, extracellular matrix, axons and nerve terminals. These nerve terminals occur throughout the central neuropile and are characterized by dense pyramidal presynaptic specializations and postsynaptic subsurface cisternae. The nervous system ofPeripatus is relatively simple in its organization, in the lack of glial intercellular junctions and in the ready accessibility of substances from the external milieu.
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References
Abbott, N. J. (1979) Primitive forms of brain homeostasis.Trends in Neurosciences2, 91–3.
Ashhurst, D. E. &Bailey, A. J. (1980) Locust collagen: morphological and biochemical characterization.European Journal of Biochemistry103, 75–83.
Ashhurst, D. E. &Costin, N. M. (1971) Insect mucosubstances. II. The mucosubstances of the central nervous system.Journal of Histochemistry3, 297–310.
Atwood, H. L. &Morin, W. A. (1970) Neuromuscular and axo-axonal synapses of the crayfish opener muscle.Journal of Ultrastructure Research32, 351–69.
Baccetti, B. (1967) Collagen of the earthworms.Journal of Cell Biology34, 885–91.
Balfour, F. M. (1883) The anatomy and development ofPeripatus capensis.Quarterly Journal of Microscopical Science23, 213–59.
Binnington, K. C. &Lane, N. J. (1980) Perineurial and glial cells in the tickBoophilus microplus. Freeze-fracture and tracer studies.Journal of Neurocytology9, 343–62.
Bullock, T. H. &Horridge, G. A. (1965)Structure and Function in the Nervous System of Invertebrates. San Francisco and London: W. H. Freeman.
Campiglia, S. (1969) Tegumento, muda e ciclo de intermuda emPeripatus acacio Marcus e Marcus (Onicoforo).Tese de Doutoramento, Universidade São Paulo, 194 p.
Coggeshall, R. E. &Fawcett, D. W. (1964) The fine structure of the CNS of the leech,Hirudo medicinalis.Journal of Neurophysiology27, 229–89.
Cuenot, L. (1949) Les Onychophores. InTraite de Zoologie, Vol. VI P-P Grasse (Dir) pp. 3–37. Paris: Masson et Cie.
Dallai, R. &Giusti, F. (1979) The epithelial cell junctions in Onychophora. InMyriapod Biology (edited byCamatini, M.), pp. 433–43. New York: Academic Press.
Del Castillo, J. &Hoyle, G. (1982) Spontaneous junctional potentials associated with cholinergic transmission inPeripatus muscle.Comparative Biochemistry and Physiology73, 451–6.
Eakin, R. M. &Westfall, J. A. (1964) Electron microscopy of photoreceptors in two species of Onychophora.American Zoologist4, 434.
Ewer, D. W. &Van Den Berg, R. (1954) A note on the pharmacology of the dorsal musculature ofPeripatopsis.Journal of Experimental Biology31, 496–500.
Federow, B. (1926) Zur Anatomie des Nervensystems vonPeripatus.Zoologische Jahrbucher (Anatomie)48, 273–310.
Federow, B. (1929) Zur Anatomie des Nervensystems vonPeripatus.Zoologische Jahrbucher (Anatomie)50, 279–332.
Florey, E. &Florey, E. (1965) Cholinergic neurons in the Onychophora: a comparative study.Comparative Biochemistry and Physiology,15, 125–36.
Gabe, M. (1954) Sur l'existence de cellules neurosecretrices chez quelques Onychopores.Comptes Rendue de l'Academie des Sciences, Paris238, 272–4.
Gaffron, E. (1885) Beitrage zur Anatomie und Histologie vonPeripatus.Zoologische Beitrung Breslau1, 33–60.
Gardner, C. R. &Robson, E. A. (1978) A response to monoamines inPeripatopsis moseleyi (Onychophora).Experientia34, 1576.
Gardner, C. R., Robson, E. A. &Stanford, C. (1978) The presence of monoamines in the nervous system ofPeripatopsis (Onychophora).Experientia34, 1577.
Hackman, R. H. &Goldberg, M. (1975) Peripatus: its affinities and its cuticle.Science190, 582–3.
Hanström, B. (1935) Bemerkungen uber das Gehirn und die Sinnesorgane der Onychoporen.Lunds Universitets Arsskrift NF, Advances 2, Bildung. 31, number 5, pp. 1–37.
Harrison, J. B. &Lane, N. J. (1981) Lack of restriction at the blood-brain interface inLimulus despite atypical junctional arrangements.Journal of Neurocytology10, 233–50.
Henry, L. M. (1948) The nervous system and the segmentation of the head in the Annulata. V. Onychophora.Microentomology13, 27–48.
Heuser, J. E. &Doggenweiler, C. F. (1966) The fine structural organization of nerve fibers, sheaths and glial cells in the prawn,Palaemonetes vulgaris.Journal of Cell Biology30, 381–403.
Holmgren, N. (1916) Zur Vergleichenden Anatomie des Gehirns von Polychaeten, Onychopores, Xiphosuren, Arachniden, Crustacen, Myriapoden und Insecten.Kungliga Svenska Vetenskapsatademiens Handlingar56, 1–103.
Hoyle, G. &Del Castillo, J. (1979) Neuromuscular transmission inPeripatus.Journal of Experimental Biology83, 13–29.
Hoyle, G. &Williams, M. (1980) The musculature ofPeripatus and its innervation.Philosophical Transactions of the Royal Society of London288, 481–510.
Hoyle, G., Williams, M. &Phillips, C. (1986) Functional morphology of insect neuronal cell-surface/ glial contacts; the trophosphongium.Journal of Comparative Neurology246, 113–28.
Lane, N. J. (1972) Fine structure of a lepidopteran nervous system and its accessibility to peroxidase and lanthanum.Zeitschrift für Zellforschung und mikroskopische Anatomie131, 205–22.
Lane, N. J. (1981a) Tight junctions in arthropod tissues.International Review of Cytology73, 243–318.
Lane, N. J. (1981b) Invertebrate neuroglia: junctional structure and development.Journal of Experimental Biology95, 7–33.
Lane, N. J. (1984) A comparison of the construction of intercellular junctions in the CNS of vertebrates and invertebrates.Trends in Neurosciences7, 95–9.
Lane, N. J. (1985) Structure of components of the nervous system. InComprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 5,Nervous System: Structure and Motor Function (edited byKerkut, G. A. &Gilbert, L. I.), pp. 1–47. Oxford: Pergamon Press.
Lane, N. J. &Abbott, N. J. (1975) The organisation of the nervous system in the crayfishProcambarus clarkii, with emphasis on the blood-brain interface.Cell and Tissue Research156, 173–87.
Lane, N. J. &Campiglia, S. S. (1985) Lack of restriction to tracer entry at the blood-brain interface ofPeripatus, the arthropod/annelid intermediate.Journal of Cell Biology101, 127a.
Lavallard, R. (1975) Connées ultrastructurales sur les organes segmentaires dePeripatus acacioi Marcus et Marcus (Onychophora: Peripatidae).Annales des Sciences naturelles, Zoologie3, 23–62.
Lavallard, R. (1977) Paroi tegumentaire et cycle d'intermue chezPeripatus acacioi Marcus et Marcus (Onychophora).Editions du CNRS, Paris, p. 153.
Lavallard, R. (1981) Données ultrastructurales sur les organes segmentaires dePeripatus acacioi Marcus et Marcus (Onychophora: Peripatidae).Annales des Sciences naturelles, Zoologie, 13 Serie,3, 23–62.
Lavallard, R. (1986) Stockage et épuisement des substances de réserve dans l'epithélium mésentérique dePeripatus acacioi Marcus et Marcus (Onychophora: Peripatidae): étude infrastructurale.Comptes rendus de l'Academie des Sciences, Paris302, Serie III No. 3, 97–102.
Lavallard, R. &Campiglia, S. S. (1979) Données ultrastructurales sur des zones synaptiques dans les néphridies dePeripatus acacioi Marcus et Marcus (Onychophora).Bolléttino de Fisiologia animal, Universidade de Sao Paulo3, 145–56.
Manton, S. M. (1973) Arthropod phylogeny — a modem synthesis.Journal of Zoology (London)173, 111–30.
Marcus, E. &Marcus, E. (1955) A newPeripatus from Minas Gerais, Brazil.Anais da Academia brasileirade dencias27, 189–93.
Mellon, D., Treherne, J. E., Lane, N. J., Harrison, J. B. &Langley, C. K. (1980) Electrical interactions between the giant axons of a polychaete worm (Sabella penicillus L.).Journal of Experimental Biology84, 119–36.
Osborne, M. P. (1975) The ultrastructure of nerve-muscle synapses. InInsect Muscle (edited byUsherwood, P. N. R.), pp. 151–205. New York: Academic Press.
Pflugfelder, O. (1955) Die Tracheen der Onychophoren und der Insekten.Mikrokosmos, 169–71.
Pflugfelder, O. (1968) Onychopora. InGrosses Zoologisches Praktikum (edited byCzihak, G.) Vol. 13a, pp. 1–42. Stuttgart: G. Discher.
Radojcic, T. &Pentreath, V. W. (1979) Invertebrate glia.Progress in Neurobiology12, 115–99.
Robson, E. A. (1964) The cuticle ofPeripatopsis moseleyi.Quarterly Journal of Microscopial Science105, 281–99.
Roots, B. I. (1978) A phylogenetic approach to the anatomy of glia. InDynamic Properties of dial Cells (edited bySchoffeniels, E. et al.) pp. 45–54. New York: Pergamon Press.
Roots, B. I. &Lane, N. J. (1983) Myelinating glia of earthworm giant axons: thermally induced intramembranous changes.Tissue and Cell15, 695–709.
Rosenberg, V. J. &Seifert, G. (1978) Fine structure of the innervation of the dorsal vessel ofPeripatoides leuckarti (Sanger, 1869).Zoologischer Anzeiger de Jena201, 521–30.
Rosenbluth, J. (1972) Myoneural junctions of two ultrastructurally distinct types in earthworm body muscle.Journal of Cell Biology54, 566–79.
Saint Remy, G. (1890) Contribution a l'étude du cerveau chez les Arthropodes Tracheates.Archives de Zoologie expérimentale et générale, Paris, 1–274.
Sanchez, S. (1958) Cellules neurosecretrices et organes-infracerebraux dePeripatopsis moseleyi Wood (Onychophores) et neurosecretion chez Nymphae gracile Leach (Pycnagonides).Archives de Zoologie expérimentale et générale, Paris96, No. 7.
Sanger, H. (1869)Peripatus capensis Gr. andPeripatus leuckartii n.sp. Trav. II Cong. nat., Moscou, p. 239–62.Transactions de le Bulletin de la Société philomathique de Paris (1901)ser.3, 9–36.
Schürmann, F. W. (1978a) A note on the structure of synapses in ventral nerve cord of the onychophoranPeripatoides leuckartii.Cell and Tissue Research186, 527–34.
Schürmann, F. W. (1978b) On the ultrastructure of nerve-muscle contacts in Onychophora.Experientia34, 779.
Schürmann, F. W. &Sandeman, D. C. (1976) Giant fibres in the ventral nerve cord ofPeripatoides leuckarti (Onychophora).Die Naturwissenshaften63, 580–1.
Smith, D. S. &Treherne, J. E. (1963) Functional aspects of the organization of the insect nervous system.Advances in Insect Physiology1, 401–84.
Snodgrass, R. E. (1938) The evolution of the Annelida, Onychophora and Arthropoda.Smithsonian Miscellaneous Collections97(6), 1–59.
Vale, R. D., Reese, T. S. &Sheetz, M. P. (1985) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility.Cell42, 39–50.
Wigglesworth, V. B. (1960) The nutrition of the central nervous system in the cockroachPeriplaneta americana L.Journal of Experimental Biology37, 500–12.
Wood, M. R., Pfenninger, K. H. &Cohen, M. J. (1977) Two types of presynaptic configurations in insect central synapsis: an ultrastructural analysis.Brain Research130, 25–45.
Zacher, F. (1933) Onychophora. InHandbuch der Zoologie (edited byKukenthal, W. &Krumbach, T.) pp. 79–138. Berlin and Leipzig: W. de Gruyter.
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Lane, N.J., Campiglia, S.S. The lack of a structured blood-brain barrier in the onychophoranPeripatus acacioi . J Neurocytol 16, 93–104 (1987). https://doi.org/10.1007/BF02456701
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DOI: https://doi.org/10.1007/BF02456701