Skip to main content
SpringerLink
Log in

The wiring-in of neural nets revisited

  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

Earlier and some recent ideas about the possible modes of specification of the wiring-in of nervous systems are reviewed in the light of older and several recent experiments, and some new ideas are suggested. It is argued that certain general principles, notably the postulated ‘principle of alternative matching’ (PALMA) and a suggested and related ‘kaleidoscopic effect’ (KALEF), as well as the notion of an ‘extracellular guidance network’ (ECGN), are in good agreement with recent and older findings concerning axonal guidance during neural wiring-in. It seems possible that by means of genetically programmed processes, neurons become systematically combinatorially labelled to such a degree that possibly all neurons areuniquely specified, as regards the combination oftypes of cell labels they make. Yet, there remains considerable freedom as regards the modes of arrangements of cell labels within cell surface membranes and the KALEF permits to overcome apparent difficulties that confronted earlier versions of the cell labelling hypotheses (cf. Edelman,Science 219, 450–457, 1983, for mention of such difficulties). Apart from label specification, neural development seems to depend on trophic factors, which are also essential for the maintenance of the developed nervous system. The systematic programmes for cell labelling, apart from generating all the required neurons, also produces inappropriate neurons and synaptic connections. These are got rid of by systematic cell death and/or atrophy of inappropriate synapses and/or elimination of inappropriate axon collaterals. The resulting neural net seems then very specifically wired-in for each species, apparently without redundant neurons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature

  • Amari, S. and M. A. Arbib (Eds.) 1982.Competition and Cooperation in Neural Nets. Lecture Notes in Biomathematics, Vol. 45. Berlin: Springer-Verlag.

    MATH  Google Scholar 

  • Andersen, P. and S. A. Andersson. 1968.Physiological Basis of the Alpha Rhythm. New York: Appleton-Century-Croft.

    Google Scholar 

  • Anninos, P. and M. Kokkinidis. 1984. “A Neural Net Model for Multiple Memory Domains.”J. theor. Biol. 109, 95–110.

    Article  MathSciNet  Google Scholar 

  • Barnstable, C. J. 1980. “Monoclonal Antibodies which Recognize Different Cell Types in the Rat Retina.”Nature, Lond. 286, 231–235.

    Article  Google Scholar 

  • Baylor, D. A. and J. G. Nicholls. 1971. “Patterns of Recognition Between Individual Nerve Cells in the Central Nervous System of the Leech.”Nature, Lond. 232, 268–270.

    Article  Google Scholar 

  • Bentley, D. and M. Caudy. 1983. “Pioneer Axons Lose Directed Growth After Selective Killing of Guide Post Cells.”Nature, Lond. 304, 62.

    Article  Google Scholar 

  • Berg, D. K. 1982. “Cell Death in Neuronal Development. Regulation by Trophic Factors.” InNeuronal Development, N. C. Spitzer, (Ed.), pp. 297–331. New York: Plenum Press.

    Google Scholar 

  • Berry, M. 1974. “Development of the Cerebral Neocortex of the Rat.” InAspects of Neurogenesis, Studies on the Development of Behavior and the Nervous System, Vol. 2, G. Gottlieb (Ed.), pp. 7–67. New York: Academic Press.

    Google Scholar 

  • Brenneman, D. E., S. Fitzgerald and P. G. Nelson. 1984. “Interaction Between Trophic Action and Electrical Activity in Spinal Cord Cultures.”Devl Brain Res. 15, 211–217.

    Article  Google Scholar 

  • Clowes, J. S. and G. D. Wassermann. 1984. “Genetic Control Theory of Developmental Events.”Bull. math. Biol. 46, 785–825.

    Article  MATH  Google Scholar 

  • Cowan, W. M., J. W. Fawcett, D. D. M. O'Leary and B. B. Stanfield. 1985. “Regressive Events in Neurogenesis.”Science 225, 1258–1265.

    Google Scholar 

  • Cragg, B. G. 1967. “The Density of Synapses and Neurones in the Motor and Visual Areas of the Cerebral Cortex.”J. Anat. 101, 639–654.

    Google Scholar 

  • —. 1968. “Are There Structural Alterations in Synapses Related to Functioning?.”Proc. R. Soc. B171, 319–323.

    Google Scholar 

  • Cunningham, T. J. 1982. “Naturally Occurring Neuron Death and Its Regulation by Developing Neural Pathways.”Int. Rev. Cytol. 74, 163–186.

    Article  Google Scholar 

  • Da Silver Lopes, F. H., T. H. M. I. van Lieropes, C. F. Schrifer and W. Storm van Leeuren. 1973. “Organisation of Thalamic and Cortical Alpha Rhythms, Spectra and Coherences.”Electroenceph. clin. Neurophysiol. 35, 672.

    Google Scholar 

  • Davies, A. M. and R. M. Lindsay. 1984. “Neural Crest-derived Spinal and Cranial Sensory Neurones are Equally Sensitive to NGF but Differ in Their Response to Tissue Extracts.”Devl Brain Res. 14, 121–127.

    Article  Google Scholar 

  • De Long, G. R. and A. J. Coulombre. 1968. “The Specificity of Retinotectal Connections Studies by Retinal Grafts Onto the Optic Tectum in Chick Embryos.”Devl Biol. 16, 513–531.

    Google Scholar 

  • Dodd, J., D. Solter and T. M. Jessell. 1984. “Monoclonal antibodies against carbohydrate differentiation antigens identify subsets of primary sensory neurones.”Nature, Lond. 311, 469–472.

    Article  Google Scholar 

  • Edelman, G. M. 1983. “Cell Adhesion Molecules.”Science 219, 450–457.

    Google Scholar 

  • — and L. M. Finkel. 1983. “Neuronal group selection in the cerebral cortex.” InDynamic Aspects of Neocortical Function, 1st Symposium of the Neuroscience Institute, La Jolla, Calif, October 1982, G. M. Edelman, W. M. Cowan and U. E. Gall (Eds.) New York: Wiley.

    Google Scholar 

  • Eisen, J. S., P. Z. Myers and M. Westerfield. 1986. “Pathway Selection by Growth Cones of Identified Motoneurones in Live Zebra Fish Embryos.”Nature, Lond. 320, 269–271.

    Article  Google Scholar 

  • Ellul, R. 1972. “The Genesis of the EEG.” InInternational Review of Neurobiology, C. C. Pfeiffer and C. C. Smythes (Eds.) London: Academic Press.

    Google Scholar 

  • Fraser, S. 1980. “Differential Adhesion Approach to the Patterning of Nerve Connections.”Devl Biol. 79, 453–464.

    Article  Google Scholar 

  • Gaze, R. M. 1970.The Foundation of Nerve Connections. London: Academic Press.

    Google Scholar 

  • —, M. J. Keating and S. H. Chung. 1974. “The Evolution of the Retinotectal Map During Development ofXenopus.”Proc. R. Soc. B185, 301–330.

    Google Scholar 

  • Geschwind, N. and W. Levitsky. 1968. “Human Brain: Left-Right Asymmetries in Temporal Speech Region.”Science 161, 186–187.

    Google Scholar 

  • Goodman, C. S., M. J. Bastiani, C. Q. Doe, S. du Lac, S. L. Helfand, J. Y. Kuwada and J. B. Thomas. 1984. “Cell Recognition During Neuronal Development.”Science 225, 1271–1279.

    Google Scholar 

  • Griffith, J. S. 1971.Mathematical Neurobiology. London: Academic Press.

    MATH  Google Scholar 

  • Guillery, R. W. and J. H. Kaas. 1971. «A Study of Normal and Congenitally Abnormal Retinogeniculate Projections in Cats.”J. comp. Neurol. 143, 73–100.

    Article  Google Scholar 

  • Hamburger, V. and R. W. Oppenheim. 1982. “Naturally occurring neuronal death in vertebrates.”Neurosci. Comment. 1, 39–55.

    Google Scholar 

  • Harris, W. A. 1981. “Neural Activity and Development.”A. Rev. Physiol. 43, 689–710.

    Article  Google Scholar 

  • Harris, W. A. 1986. “Homing Behaviour of Axons in the embryonic Vertebrate Brain.”Nature, Lond. 320, 266–267.

    Article  Google Scholar 

  • Haun, F. and T. J. Cunningham. 1984. “Cortical Transplants Reveal CNS Trophic Interactions inSitu.”Devl Brain Res. 15, 290–294.

    Article  Google Scholar 

  • Hawkes, R., E. Nirday and A. Matus. 1982. “Monoclonal Antibodies Identify Novel Neural Antigens.”Proc. natn. Acad. Sci. U.S.A. 79, 2410–2414.

    Article  Google Scholar 

  • Heuschert, D. 1963. “EEG-Untersuchungen an eineiigen Zwillingen im höheren Lebensalter.”Z. mensch. Vererb.-u. Konstit Lehre 37, 128.

    Google Scholar 

  • Ho, R. K. and C. S. Goodman. 1982. “Peripheral Pathways are Pioneered by an Array of Central and Peripheral Neurones in Grasshopper Embryos.“Nature, Lond. 297, 404.

    Article  Google Scholar 

  • Hope, R. A., B. J. Hammond and R. M. Gaze. 1976. “The Arrow Model: Retinotectal Specificity and Map Formation in the Goldfish Visual System.”Proc. R. Soc. B194, 447–466.

    Article  Google Scholar 

  • Hubel, D. H. and T. N. Wiesel. 1971. “Abberant Visual Projection in the Siamese Cat.”J. Physiol.,218, 33–62.

    Google Scholar 

  • Hunt, R. K. and M. Jacobson. 1974. “Neuronal specificity revisited.”Curr. Top. Devl Biol.,8, 203–259.

    Article  Google Scholar 

  • Jacobson, M. 1970.Developmental Neurobiology (1st edn.) New York: Holt Rinehart.

    Google Scholar 

  • Jacobson, M. 1978.Developmental Neurobiology (2nd edn.) New York: Plenum Press.

    Google Scholar 

  • Jacobson, M. and Hunt, R. K.. 1973. “The Origins of Nerve-cell Specificity.”Scient. Am.,228, No. 2, pp. 26–35.

    Article  Google Scholar 

  • Jirikowski, G., I. Reisert and C. Pilgrim. 1984. “Angiotensin II Promotes Development of neurophysin in Neurons in Dissociated Culture.”Devl Brain Res. 14, 179–183.

    Article  Google Scholar 

  • Kalil, R. E., S. R. Jhaveri and W. Richards. 1971. “Anomalous Retinal Pathways in the Siamese Cat: an Inadequate Substrate for Normal Binocular Vision.”Science 174, 302–305.

    Google Scholar 

  • Kiloh, L. G., A. J. McComas and J. W. Osselton. 1972.Clinical Electroencephalography. London: Butterworth.

    Google Scholar 

  • Koch, G. 1967. “Epilepsien.” InHumangenetik, P. E. Becker (Ed.), Vol. V, part 2, pp. 1–83. Stuttgart: Thieme.

    Google Scholar 

  • Landis, S. C. 1983. “Neuronal Growth Cones.”A. Rev. Physiol.,45, 567–587.

    Article  Google Scholar 

  • Laties, A. M. and J. M. Sprague. 1966. “The Projection of Optic Fibers to the Visual Centers in the Cat.”J. comp. Neurol. 127, 35–70.

    Article  Google Scholar 

  • Lenneberg, E. H. 1970. InThe Neurosciences Second Study Program, F. O. Schmitt (Ed.), p. 361 ff. New York: Rockefeller University Press.

    Google Scholar 

  • Lennox, W. G., E. L. Gibbs and F. A. Gibbs. 1945. “The Brain Wave Pattern: a Hereditary Trait. Evidence from 74 ‘Normal’ Pairs of Twins.”J. Hered. 36, 233.

    Google Scholar 

  • Lorber, J. 1981. “The Disposable Cortex.”Psychol. Today 15, 126.

    Google Scholar 

  • Lyser, K. M. 1966. “The Development of the Chick Embryo Diencephalon and Mesencephalon During the Initial Phases of Neuroblast Differentiation.”J. Embryol. exp. Morphol. 16, 497–517.

    Google Scholar 

  • McKay, R., M. C. Raff and L. F. Reichardt (Eds.) 1981.Cold Spring Harbor Reports in the Neurosciences, Vol. 2.Monoclonal Antibodies to Neural Antigens. New York: Cold Spring Harbor.

    Google Scholar 

  • Mallet, J., R. Christen and P. J. Changeux. 1979. “Immunological Studies on the Purkinje Cells from Rat and Mouse Cerebella. I. Evidence for Antibodies Characteristic of Purkinje Cells.”Devl Biol. 72, 308–319.

    Article  Google Scholar 

  • Morest, D. K. 1968. “The Growth of Synaptic Endings in the Mammalian Brain: a Study of the Calyses of the Trapezoid Body.”Z. Anat. EntwGesch. 127, 201–220.

    Article  Google Scholar 

  • —. 1969. “The Differentiation of Cerebral Dendrites: a Study of the Post-migratory Neuroblast in the Medial Nucleus of the Trapezoid Body.”Z. Anat. EntwGesch. 128, 271–289.

    Article  Google Scholar 

  • Needham, J. 1942.Biochemistry and Morphogenesis. Cambridge: Cambridge University Press.

    Google Scholar 

  • Nieuwkoop, P. D. and J. Faber. 1956.Normal Tables of Xenopus laevis. Amsterdam: Elsevier, North Holland.

    Google Scholar 

  • Nottebohm, F. 1980. “Testosterone Triggers Growth of Brain Vocal Control Nuclei in Adult Female Canaries.”Brain Res. 189, 429–436.

    Article  Google Scholar 

  • Oppenheim, R. W. 1981. “Neuronal Cell Death and Some Related Regressive Phenomena during Neurogenesis: a Selective Historical Review and Progress Report.” InStudies in Developmental Neurobiology, W. M. Cowan (Ed.), pp. 74–133. New York: Oxford University Press.

    Google Scholar 

  • Osato, S. and I. Awano. 1957. “Genetische Studien an Zwillingen.”Acta Geneticae et Gemellolologiae (Roma)6, 283–366.

    Google Scholar 

  • Overton, K. J. and M. A. Arbib. 1982a. “Systems Matching and Topographic Maps: the Branch-Arrow Model (BAM).” InCompetition and Cooperation in Neural Nets, S. Amari and M. A. Arbib (Eds), pp. 202–225. Lecture Notes in Biomathematics, Vol. 45. Berlin: Springer Verlag.

    Google Scholar 

  • — and —. 1982b. “The Extended Branch-arrow Model of the Formation of Retinotectal Connections.”Biol. Cybernet.,45, 157–176.

    Article  Google Scholar 

  • Palay, S. L. 1967. “Principles of Cellular Organization in the Nervous System.” InThe Neurosciences A Study Program, G. C. Quarton, T. Melnechuk and F. O. Schmitt (Eds.) New York: Rockefeller University Press.

    Google Scholar 

  • Rappelsberger, P., H. Pockberger and H. Petsche. 1982. “The Contribution of the Cortical Layers to the Generation of the EEG: Field Potential and Current Source Density Analysis in the Rabbit's Visual Cortex.”Electroenceph. clin. Neurophysiol.,53, 254–269.

    Article  Google Scholar 

  • Reeber, A., G. Vincendon and J. P. Zanetta. 1981. “Isolation and Immunohistochemical Localization of a Purkinje Cell Specific Glycoprotein Subunit from Rat Brain Cerebellum.”Brain Res. 229, 53–65.

    Article  Google Scholar 

  • Riopelle, R. J. and D. A. Cameron. 1984. “Neurite-promoting Factors from Embryonic Neurons.”Devl Brain Res. 15, 265–274.

    Article  Google Scholar 

  • Robertson, M. 1982. “Learning, Forgetting and the Cell Biology of Memory.”Nature, Lond. 300, 219–220.

    Article  Google Scholar 

  • Rose, S. 1976.The Conscious Brain (rev. edn.) Harmondsworth: Penguin Books.

    Google Scholar 

  • Roseman, S. 1974a. “The Biosynthesis of Cell Surface Components and their Potential Role in Intercellular Adhesion.” InThe Neurosciences Third Study Program, F. O. Schmitt and F. G. Worden (Eds), pp. 795–804. Cambridge, MA: MIT Press.

    Google Scholar 

  • — 1974b. “Complex Carbohydrates and Intercellular Adhesion.” InThe Cell Surface in Development, A. A. Moscona (Ed.), pp. 255–271. New York: Wiley.

    Google Scholar 

  • Sanes, J. R. 1983. “Roles of Extracellular Matrix in Neural Development.”A. Rev. Physiol.,45, 581–600.

    Article  Google Scholar 

  • — 1984. “More Nerve Growth Factors?”Nature, Lond. 307, 500.

    Article  Google Scholar 

  • Schnitzer, J., S. U. Kim and M. Schachner. 1984. “Specificity of Monoclonal Antibody N1 for Cell Surfaces of Mouse Central Nervous System Neurons.”Devl Brain Res. 15, 21–32.

    Article  Google Scholar 

  • Scott, D. 1976.Understanding EEG. London: Duckworth.

    Google Scholar 

  • Sharma, S. C. 1972. “Retinotectal Connexions of a Heterotopic Eye.”Nature New Biol. 238, 286–287.

    Article  Google Scholar 

  • Sholl, D. A. 1956.The Organization of the Cerebral Cortex. London: Methuen.

    Google Scholar 

  • Sperry, R. W. 1944. “Optic nerve regeneration with return of vision in Anurans”J. Neurophysiol. 7, 59–69.

    Google Scholar 

  • — 1945. “Restoration of Vision After Crossing of Optic Nerves and After Contralateral Transplantation of Eye.”J. Neurophysiol. 8, 15–28.

    Google Scholar 

  • — 1955. InBiochemistry of the Developing Nervous System, H. Waelsch (Ed.). New York: Academic Press.

    Google Scholar 

  • — 1963. “Chemoaffinity in the orderly growth of nerve patterns and connections.”Proc. natn. Acad. Sci. U.S.A.,50, 701–709.

    Article  Google Scholar 

  • — and E. Hibbard. 1968. “Regulative factors in the orderly growth of retino-tectal connexions.” InGrowth of the Nervous System, Ciba Foundation Symposium, G. E. W. Wolstenholme and M. O'Connor (Eds), pp. 41–52. London: Churchill.

    Google Scholar 

  • Springer, S. P. and G. Deutsch 1981.Left Brain Right Brain. San Francisco: W. H. Freeman.

    Google Scholar 

  • Stone, J. and S. M. Hansen. 1966. “The Projection of the Cat's Retina on the Lateral Geniculate Nucleus.”J. comp. Neurol. 126, 601–624.

    Google Scholar 

  • Straznicky, K., R. M. Gaze and M. J. Keating. 1971. “The Retinotectal Projections after Uncrossing The Optic Chiasma inXenopus with One Compound Eye.”J. Embrol. exp. Morphol. 26, 523–542.

    Google Scholar 

  • Szentágothai, J. and G. Székely. 1956. “Zum Problem der Kreuzung von Nervenbahnen.”Acta Biol. Acad. Sci. Hung. 6, 215–229.

    Google Scholar 

  • Traynor, A. E. and D. Schubert. 1984. “Phospholipases Elevate Cyclic AMP Levels and Promote Neurite Extensions in a Clonal Nerve Cell Line.”Devl Brain Res. 14, 197–204.

    Google Scholar 

  • Trisler, D. 1982. “Are Molecular Markers of Cell Position Involved in the Formation of Neural Circuits?”Trends Neurosci. 5, 306–310.

    Article  Google Scholar 

  • Vogel, F. 1958. “Über die Erblichkeit des normalen Elektroenzephalogramms: Vergleichende Untersuchungen an ein-und zwei-eiigen Zwillingen. Stuttgart: Thieme.

    Google Scholar 

  • Vogel, F. 1963. “Genetische Aspekte des Enzephalogramms.”Deutsche Medizinische Wochenschrift 88, 1748.

    Article  Google Scholar 

  • Wassermann, G. D. 1972.Molecular Control of Cell Differentiation and Morphogenesis. New York: Marcel Dekker.

    Google Scholar 

  • — 1973. “Molecular Genetics and Developmental Biology.”Nature New Biol. 245, 163–165.

    Article  Google Scholar 

  • —. 1978.Neurobiological Theory of Psychological Phenomena. London: Macmillan.

    Google Scholar 

  • Willshaw, D. J. and C. Von der Malsburg. 1979. “A Marker Induction Mechanism for the Establishment of Ordered Neural Mappings: Its Application to the Retinotectal Problem.”Phil. Trans. R. Soc. B287, 303–343.

    Google Scholar 

  • Wilson, H. R. and J. D. Cowan. 1973. “A Mathematical Theory of the Functional Dynamics of Cortical and Thalamic Nervous Tissue.”Kybernetik 13, 55–80.

    Article  MATH  Google Scholar 

  • Zaimis, E. (Ed.) 1972.Nerve Growth Factor and its Antiserum. London: The Athlone Press of the University of London.

    Google Scholar 

  • Zipser, B. and R. McKay. 1981. “Monoclonal Antibodies Distinguish Identifiable Neurones in the Leech.”Nature, Lond. 289, 549–554.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. University of Newcastle upon Tyne, NE1 7RU, Newcastle upon Tyne, U.K.

    G. D. Wassermann

Authors
  1. G. D. Wassermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wassermann, G.D. The wiring-in of neural nets revisited. Bltn Mathcal Biology 48, 661–680 (1986). https://doi.org/10.1007/BF02462329

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02462329

Keywords

Search

Navigation