Abstract
A theory of projections in the nervous system (such as the retino-tectal projection) is proposed. Components of axonal growth cones and target tissue interact and cooperate, within the area of contact, to generate a guiding parameter, in the simplest case a “guiding substance” of distributionp. The components which are involved in this production are assumed to have graded distributions with respect to position in the projecting and target area, respectively. The distributionp thus produced guides the growth cone in the direction of maximal slope until the minimal value ofp is reached. In this way, each growth cone can be guided to a position on the target tissue which depends on the origin of the fiber in such a manner that a projection results. Adhesive forces could but need not be involved in the guiding mechanism. The slope ofp may interfere with an intracellular pattern forming mechanism within the growth cone, determining the polarity of activation (as modelled previously on the basis of autocatalysis and lateral inhibition) and thus the direction of growth. For the generation of a distribution ofp leading to a reliable projection, simple graded distributions in the projecting and target area suffice, involving one or two components in each dimension. Their effect on the generation ofp may be activatory as well as inhibitory. Exponential gradients give rise to particularly simple mapping functions. The following is an example of this general type of model: Growth cones as well as target tissue contribute to the production of a guiding substance. For each dimension, there is, in the target tissue, an exponentially graded component exerting (directly or indirectly) two functions: it actively produces guiding substancep and it interacts, in an inhibitory fashion, with the production ofp by a component of the growth cone (which is, in turn, graded with respect to position of origin in the projecting area). While the theory is proposed as a fair approximation of the primary events in neural projections, superimposed regulatory effects can also be incorporated. These include fiber-fiber interactions, mechanisms smoothing out unequal density distributions of axon terminals and effects of time of arrival of fibers on the projection, which have been proposed previously as primary mechanisms generating projections. A further extension of the model is to assume that crude and more refined positional specificity is determined in a combinatorial fashion, allowing the possibility of interchanges and transformations of parameters.
Similar content being viewed by others
References
Bonhoeffer, F., Huf, J.: Recognition of cell types by axonal growth cones in vitro. Nature288, 162–164 (1980)
Bonner, J.T.: Evidence for the formation of cell aggregates by chemotaxis in the development of the slime moldDictyostelium discoideum. J. exp. Zool.106, 1–26 (1947)
Cowan, W.M.: Aspects of Neural Development. Int. Rev. Physiol. Neurophysiol. III17, 149–189 (1978)
Fraser, S.E.: A differential adhesion approach to the patterning of nerve connection. Dev. Biol.79, 453–464 (1980)
Fujisawa, H.: Retinotopic analysis of fiber pathways in the regenerating retinotectal system of the adult newtCynops pyrrhogaster. Brain Res.206, 27–37 (1981)
Fujisawa, H., Watanabe, K., Tani, N., Ibata, Y.: Retinotopic analysis of fiber pathways in amphibians. I. The adult newtCynops pyrrhogaster. Brain Res.206, 9–20 (1981a)
Fujisawa, H., Watanabe, K., Tani, N., Ibata, Y.: Retinotopic analysis of fiber pathways in amphibians. II. The frogRana nigromaculata. Brain Res.206, 21–26 (1981b)
Gaze, R.M., Sharma, S.C.: Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve fibres. Exp. Brain Res.10, 171–181 (1970)
Gerisch, G.: Stadienspezifische Aggregationsmuster beiDictyostelium discoideum. Wilhelm Roux Arch. Entwicklungsmech. Org.156, 127–144 (1965)
Gierer, A., Meinhardt, H.: A theory of biological pattern formation. Kybernetik12, 30–39 (1972)
Glansdorff, P., Prigogine, J.: Thermodynamic theory of structure, stability, and fluctuations. London: Wiley Interscience 1971
Gundersen, R.W., Barrett, J.N.: Neuronal chemotaxis: chick dorsalroot axons turn toward high concentrations of nerve growth factor. Science206, 1079–1080 (1979)
Halfter, W., Claviez, M., Schwarz, U.: Antero-posterior polarity in embryonic chick retina: preferential adhesion of tectal membranes to anterior axons. Nature (1981) (in press)
Jacobson, M.: Developmental neurobiology. New York, London: Plenum Press 1978
Levine, R., Jacobson, M.: Deployment of optic nerve fibers is determined by positional markers in the frog's tectum. Exp. Neurol.43, 527–538 (1974)
Meinhardt, H.: Models for the ontogenetic development of higher organisms. Rev. Physiol. Biochem. Pharmacol.80, 47–104 (1978)
Meinhardt, H., Gierer, A.: Applications of a theory of biological pattern formation based on lateral inhibition. J. Cell. Sci.15, 321–346 (1974)
Rager, G.: Morphogenesis and physiogenesis of the retinotectal connection in the chicken. II. The retino-tectal synapse. Proc. R. Soc. London. Ser. B192, 353–370 (1976)
Schmidt, J.T.: Retinal fibers alter tectal positional markers during the expansion of the half-retinal projection in goldfish. J. comp. Neurol.177, 279–299 (1978)
Schmidt, J.T., Cicerone, C.M., Easter, S.S.: Expansion of the half-retinal projection to the tectum in goldfish: an electrophysiological and anatomical study. J. comp. Neurol.177, 257–277 (1978)
Sharma, S.C.: Reformation of retinotectal projections after various tectal ablations in adult goldfish. Exp. Neurol.34, 171–182 (1972)
Sharma, S.C., Gaze, R.M.: The retinotopic organization of visual responses from tectal reimplants in adult goldfish. Arch. Ital. Biol.109, 357–366 (1971)
Sperry, R.W.: Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Nat. Acad. Sci. USA50, 703–710 (1963)
Trisler, G.D., Schneider, M.D., Nirenberg, M.: A topographic gradient of molecules in retina can be used to identify neuron position. Proc. Natl. Acad. Sci. USA78, 2145–2149 (1981)
Willshaw, D.J., von der Malsburg, C.: How patterned neural connections can be set up by self-organization. Proc. R. Soc. London, Ser. B194, 431–445 (1976)
Willshaw, D.J., von der Malsburg, C.: A marker induction mechanism for the establishment of ordered neural mappings: its applications to the retinotectal problem. Philos. Trans. R. Soc. Lond. B287, 203–243 (1979)
Yoon, M.G.: Reorganization of retinotectal projection following surgical operations on the optic tectum in goldfish. Exp. Neurol.33, 395–411 (1971)
Yoon, M.G.: Readjustment of retinotectal projection following reimplantation of a rotated or inverted tectal tissue in adult goldfish. J. Physiol. (London)252, 137–158 (1975)
Yoon, M.G.: Induction of compression in the re-established visual projections on to a rotated tectal reimplant that retains its original topographic polarity within the halved optic tectum of adult goldfish. J. Physiol. (London)264, 379–410 (1977)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gierer, A. Development of projections between areas of the nervous system. Biol. Cybern. 42, 69–78 (1981). https://doi.org/10.1007/BF00335161
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00335161