Variability of axonal arborizations hides simple rules of construction: A topological study from HRP intracellular injections

Intracellular staining with horseradish peroxidase (HRP) allows the analysis of the extent and diversity of axonal field, as the Golgi techniques did for dendritic fields. In this study, we have used such HRP injections to investigate possible rules of construction that underlie the variability in the observed morphological patterns of axons. The Mauthner cell of the teleost provides a suitable material for such a work since it receives inhibitory inputs from two distinct classes of cells that can be identified physiologically prior to their intracellular staining: those that contribute to a recurrent collateral network and those that are part of the commissural vestibuloves‐tibular pathway. The distribution of their terminal boutons over the M‐cell surface was quantified and their axonal arborizations were analyzed topologically with the help of a centripetal method of terminal ordering.

[1]  H. Hayashi Morphology of central terminations of intra‐axonally stained, large, myelinated primary afferent fibers from facial skin in the rat , 1985, The Journal of comparative neurology.

[2]  H. Vanegas,et al.  Diameters and terminal patterns of retinofugal axons in their target areas: An HRP study in two teleosts (Sebastiscus and Navodon) , 1984, The Journal of comparative neurology.

[3]  C. Stuermer Rules for retinotectal terminal arborizations in the goldfish optic tectum: A whole‐mount study , 1984, The Journal of comparative neurology.

[4]  H Korn,et al.  Transformation of binomial input by the postsynaptic membrane at a central synapse. , 1984, Science.

[5]  G. Shepherd,et al.  Synaptic excitatory and inhibitory interactions at distal dendritic sites on mitral cells in the isolated turtle olfactory bulb , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  A. I. Shapovalov,et al.  Tracing of frog sensory‐motor synapses by intracellular injection of horseradish peroxidase. , 1984, The Journal of physiology.

[7]  T. Woolsey,et al.  Computer‐assisted analyses of barrel neuron axons and their putative synaptic contacts , 1983, The Journal of comparative neurology.

[8]  B. Walmsley,et al.  Amplitude fluctuations in synaptic potentials evoked in cat spinal motoneurones at identified group Ia synapses. , 1983, The Journal of physiology.

[9]  H. Korn,et al.  Transmission at a central inhibitory synapse. III. Ultrastructure of physiologically identified and stained terminals. , 1982, Journal of neurophysiology.

[10]  C. Mason Development of terminal arbors of retino-geniculate axons in the kitten—I. Light microscopical observations , 1982, Neuroscience.

[11]  H. Korn,et al.  Morphologically distinct classes of inhibitory synapses arise from the same neurons: Ultrastructural identification from crossed vestibular interneurons intracellularly stained with HRP , 1981, The Journal of comparative neurology.

[12]  J. Rastad Ultrastructural morphology of axon terminals of an inhibitory spinal interneurone in the cat , 1981, Brain Research.

[13]  S. Cullheim,et al.  An ultrastructural study of the synaptic contacts ofα1-motoneuron axon collaterals. II. Contacts in lamina VII , 1981, Brain Research.

[14]  H Korn,et al.  Fluctuating responses at a central synapse: n of binomial fit predicts number of stained presynaptic boutons. , 1981, Science.

[15]  P. Rose Distribution of dendrites from biventer cervicis and complexus motoneurons stained intracellularly with horseradish peroxidase in the adult cat , 1981, The Journal of comparative neurology.

[16]  S. Cullheim,et al.  An ultrastructural study of the synaptic contacts of α-motoneurone axon collaterals. I. Contacts in lamina IX and with identified α-motoneurone dendrites in lamina VII , 1981, Brain Research.

[17]  D. Purves,et al.  Elimination of synapses in the developing nervous system. , 1980, Science.

[18]  D. Faber,et al.  An identifiable class of statoacoustic interneurons with bilateral projections in the goldfish medulla , 1980, Neuroscience.

[19]  M. Descheˆnes,et al.  Axonal branch diameter and spacing of nodes in the terminal arborization of identified thalamic and cortical neurons , 1980, Brain Research.

[20]  N. Ishizuka,et al.  Axonal branches and terminations in the cat abducens nucleus of secondary vestibular neurons in the horizontal canal system , 1980, Neuroscience Letters.

[21]  T. Hongo,et al.  Trajectory of group Ia afferent fibers stained with horseradish peroxidase in the lumbosacral spinal cord of the cat: Three dimensional reconstructions from serial sections , 1979, The Journal of comparative neurology.

[22]  T. Wiesel,et al.  Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex , 1979, Nature.

[23]  L. V. Keulen Axon trajectories of Renshaw cells in the lumbar spinal cord of the cat, as reconstructed after intracellular staining with horseradish peroxidase , 1979, Brain Research.

[24]  B. Walmsley,et al.  HRP anatomy of group la afferent contacts on alpha motoneurones , 1979, Brain Research.

[25]  D. Faber,et al.  Structural correlates of recurrent collateral interneurons producing both electrical and chemical inhibitions of the Mauthner cell , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[26]  S Cullheim,et al.  A morphological study of the axons and recurrent axon collaterals of cat sciatic α‐motoneurons after intracellular staining with horseradish peroxidase , 1978, The Journal of comparative neurology.

[27]  M. Berry,et al.  The Purkinje cell dendritic tree in mutant mouse cerebellum. A quantitative Golgi study of Weaver and Staggerer mice , 1978, Brain Research.

[28]  J. Changeux,et al.  Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks , 1976, Nature.

[29]  H Korn,et al.  Vertebrate central nervous system: same neurons mediate both electrical and chemical inhibitions. , 1976, Science.

[30]  M. Berry,et al.  The application of network analysis to the study of branching patterns of large dendritic fields , 1976, Brain Research.

[31]  M. Berry,et al.  Network analysis of dendritic fields of pyramidal cells in neocortex and Purkinje cells in the cerebellum of the rat. , 1975, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[32]  H Korn,et al.  An electrically mediated inhibition in goldfish medulla. , 1975, Journal of neurophysiology.

[33]  Y. Nakajima Fine structure of the synaptic endings on the Mauthner cell of the goldfish , 1974, The Journal of comparative neurology.

[34]  I. Parnas,et al.  Differential flow of information into branches of a single axon. , 1973, Brain research.

[35]  D. Bray BRANCHING PATTERNS OF INDIVIDUAL SYMPATHETIC NEURONS IN CULTURE , 1973, The Journal of cell biology.

[36]  D. Faber,et al.  A Neuronal Inhibition Mediated Electrically , 1973, Science.

[37]  G. J. Smit,et al.  The branching pattern in dendrites of cortical neurons. , 1972, Acta morphologica Neerlando-Scandinavica.

[38]  N. K. Wessells,et al.  ULTRASTRUCTURE AND FUNCTION OF GROWTH CONES AND AXONS OF CULTURED NERVE CELLS , 1971, The Journal of cell biology.

[39]  P. Haggett Network Analysis In Geography , 1971 .

[40]  Ruth E M Bowden,et al.  The Inhibitory Pathways of the Central Nervous System , 1970 .

[41]  M. Colonnier Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[42]  M. Karnovsky,et al.  THF EARLY STAGES OF ABSORPTION OF INJECTED HORSERADISH PEROXIDASE IN THE PROXIMAL TUBULES OF MOUSE KIDNEY: ULTRASTRUCTURAL CYTOCHEMISTRY BY A NEW TECHNIQUE , 1966, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[43]  E. Furshpan,et al.  Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. , 1962, Journal of neurophysiology.

[44]  Gray Eg Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study , 1959 .

[45]  A. N. Strahler Quantitative analysis of watershed geomorphology , 1957 .

[46]  Sholl Da Dendritic organization in the neurons of the visual and motor cortices of the cat. , 1953 .

[47]  R. Horton EROSIONAL DEVELOPMENT OF STREAMS AND THEIR DRAINAGE BASINS; HYDROPHYSICAL APPROACH TO QUANTITATIVE MORPHOLOGY , 1945 .

[48]  C. C. Speidel Studies of living nerves. VII. Growth adjustments of cutaneous terminal arborizations , 1942 .

[49]  D. Bodian The structure of the vertebrate synapse. A study of the axon endings on mauthner's cell and neighboring centers in the goldfish , 1937 .

[50]  Harry Grundfest,et al.  ACTION AND EXCITABILITY IN MAMMALIAN A FIBERS , 1936 .

[51]  G. W. Bartelmez Mauthner's cell and the nucleus motorius tegmenti , 1915 .

[52]  H. Korn What Central Inhibitory Pathways Tell Us About Mechanisms of Transmitter Release , 1984 .

[53]  A. G. Brown,et al.  The morphology of group Ia afferent fibre collaterals in the spinal cord of the cat. , 1979, The Journal of physiology.

[54]  石塚 典生 Trajectory of group 1a afferent fibers stained with horseradish peroxidase in the lumbosacral spinal cord of the cat : three dimensional reconstructions from serial sections , 1979 .

[55]  L. V. van Keulen Axon trajectories of Renshaw cells in the lumbar spinal cord of the cat, as reconstructed after intracellular staining with horseradish peroxidase. , 1979, Brain research.

[56]  K. Horsfield,et al.  Some mathematical properties of branching trees with application to the respiratory system. , 1976, Bulletin of mathematical biology.

[57]  K. Horsfield Some mathematical properties of branching trees with application to the respiratory system , 1976 .

[58]  Uylings Hb,et al.  Ordering methods in quantitative analysis of branching structures of dendritic trees. , 1975 .

[59]  S G Waxman,et al.  Integrative properties and design principles of axons. , 1975, International review of neurobiology.

[60]  R M Flinn,et al.  Application of network analysis to the study of the branching patterns of dendritic fields. , 1975, Advances in neurology.

[61]  G. J. Smit,et al.  Ordering methods in quantitative analysis of branching structures of dendritic trees. , 1975, Advances in neurology.

[62]  D. Bray,et al.  The growth cone in neurite extension. , 1973, Ciba Foundation symposium.

[63]  A. Scheibel,et al.  Of Pattern and Place in Dendrites12 , 1970 .

[64]  M. Karnovsky,et al.  A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron-microscopy , 1965 .

[65]  Lloyd Guth,et al.  Studies on vertebrate neurogenesis , 1960 .

[66]  W. R. Adey Recent studies of the rhinencephalon in relation to temporal lobe epilepsy and behavior disorders. , 1959, International review of neurobiology.

[67]  E. Gray,et al.  Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. , 1959, Journal of anatomy.

[68]  D. Sholl Dendritic organization in the neurons of the visual and motor cortices of the cat. , 1953, Journal of anatomy.

[69]  B. Frankenhaeuser [The hypothesis of saltatory conduction]. , 1952, Cold Spring Harbor symposia on quantitative biology.