Abstract
To understand the rules by which axons lay down their synaptic boutons we analyzed the linear bouton distributions in 39 neurons (23 spiny, 13 smooth) and 3 thalamic axons, which were filled intracellularly with horseradish peroxidase (HRP) during in vivo experiments in cat area 17. The variation of the total number of boutons and the total axonal length was large (789–7912 boutons, 12–126 mm). The overall linear bouton density for smooth cells was higher than that of spiny cells and thalamic afferents (mean ± sd, 110 ± 21 and 78 ± 27 boutons per mm of axonal length). The distribution of boutons varied according to their location on the tree. Distal axon collaterals (first and second order segments in Horton-Strahler ordering) of smooth neurons had a 3.5 times higher, spiny cells and thalamic afferents a 2 times higher bouton density compared to the higher order (more proximal) segments. The distribution of interbouton intervals was positively skewed and similar for cells of the same type. In most cases a γ-distribution fitted well, but the distributions had a tendency to have a heavier tail. To a first approximation these bouton distributions are consistent with both diffuse and specific models of interneuronal connections. Quite simple rules can explain these distributions and the connections between the different classes of neurons.
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Ahmed, B., Anderson, J. C., Douglas, R. J., Martin, K. A. C. &; Nelson, J. C. (1994) Polyneuronal innervation of spiny stellate neurons in cat visual cortex. Journal of Comparative Neurology 341, 39–49.
Ahmed, B., Anderson, J. C., Martin, K. A. C. &; Nelson, J. C. (1997) Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. Journal of Comparative Neurology 380, 230–242.
Amir, Y., Harel, M. &; Malach, R. (1993) Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex. Journal of Comparative Neurology 334, 19–46.
Anderson, J. C., Douglas, R. J., Martin, K. A. C. &; Nelson, J. C. (1994) Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex. Journal of Comparative Neurology 341, 16–24.
Anderson, J. C. &; Martin, K. A. C. (2001) Does bouton morphology optimize axon length? Nature Neuroscience 4, 1166–1167.
Beaulieu, C. &; Colonnier, M. (1983) The number of neurons in the different laminae of the binocular and monocular regions of area 17 in the cat. Journal of Comparative Neurology 217, 337–344.
Braitenberg, V. &; SchÜz, A. (1991) Anatomy of the Cortex. Berlin: Springer-Verlag.
Cajal, S. R. Y. (1989) Recollections of My Life. Cambridge, MA: MIT Press.
Cherniak, C. (1992) Local optimization of neuron arbors. Biological Cybernetics 66, 503–510.
Cox, D. R. &; Isham, V. (1980) Point Processes. Monographs on Applied Probability and Statistics. London, New York: Chapman and Hall.
Creutzfeldt, O. D. (1977) Generality of the functional structure of the neocortex. Naturwissenschaften 64, 507–517.
Dantzker, J. L. &; Callaway, E. M. (2000) Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nature Neuroscience 3, 701–707.
Douglas, R. J., Koch, C. K., Mahowald, M., Martin, K. A. C. &; Suarez, H. H. (1995) Recurrent excitation in neocortical circuits. Science 269, 981–985.
Douglas, R. J., Martin, K. A. C. &; Whitteridge, D. (1991)Anintracellular analysis of the visual responses of neurons in cat visual cortex. Journal of Physiology (London) 440, 659–696.
Efron, B. &; Tibshirani, R. J. (1993) An Introduction to the Bootstrap, Vol. 57 of Monographs on Statistics and Applied Probability. New York: Chapman and Hall.
Engert, F. &; Bonhoeffer, T. (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70.
Feldmeyer, D. &; Sakmann, B. (2000) Synaptic efficacy and reliability of excitatory connections between the principal neurons of the input (layer 4) and the output (layer 5) of the neocortex. Journal of Physiology 525, 31–39.
Feller, W. (1971) An Introduction to Probability Theory and Its Applications II. Wiley Series in Probability and Mathematical Statistics. John Wiley and Sons.
Freeman, W. J. (1975) Mass action in the nervous system. New York: Academic Press.
Freund, T. F., MaglÓczky, Z., Soltesz, I. &; Somogyi, P. (1986) Synaptic connections, axonal and dendritic patterns of neurons immunoreactive for cholecystokinin in the visual cortex of the cat. Neuroscience 19, 1133–1159.
Freund, T. F., Martin, K. A. C., Smith, A. D. &; Somogyi, P. (1983) Glutamate decarboxylaseimmunoreative terminals of Golgi-impregnated axo-axonic cells of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex. Journal of Comparative Neurology 221, 263–278.
Freund, T. F., Martin, K. A. C. &; Whitteridge, D. (1985a) Innervation of cat visual areas 17 and 18 by physiologically identified X-and Y-type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements. Journal of Comparative Neurology 342, 263–274.
Freund, T. F., Martin, K. A. C. &; Whitteridge, D. (1985b) Innervation of cat visual areas 17 and 18 by physiologically identified X-and Y-type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation. Journal of Comparative Neurology 342, 263–274.
Friedlander, M. J. &; Martin, K. A. C. (1989) Development of Y-axon innervation of cortical area 18 in the cat. Journal of Physiology (London) 416, 183–213.
Friedlander, M. J. &; Stanford, L. R. (1984) Effects of monocular deprivation on the distribution of cell types in the LGNd: A sampling study with fine-tipped micropipettes. Experimental Brain Research 53, 451–461.
Gabbott, P. L. A., Martin, K. A. C. &; Whitteridge, D. (1987) Connections between pyramidal neurons in layer 5 of cat visual cortex (area17). Journal of Comparative Neurology 259, 364–381.
Garey, L. J. &; Powell, T. P. (1971) An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proceedings of the Royal Society of London. Series B. Biological sciences 179, 41–63.
Gilbert, C. D. &; Wiesel, T. N. (1983) Clustered intrinsic connections in cat visual cortex. Journal of Neuroscience 3, 1116–1133.
Gonchar, Y., Turney, S., Price, J. L. &; Burkhalter, A. (2002) Axo-axonic synapses formed by somatostatin-expressing GABAergic neurons in rat and monkey visual cortex. Journal of Comparative Neurology 443, 1–14.
Hellwig, B., SchÜz, A. &; Aerstsen, A. (1994) Synapses on axon collaterals of pyramidal cells are spaced at random intervals: A Golgi study in the mouse cerebral cortex. Biological Cybernetics 71, 1–12.
Hubel, D. H. &; Wiesel, T. N. (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106–154.
Hubel, D. H. &; Wiesel, T. N. (1965) Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. Journal of Neurophysiology 28, 229–289.
Hubel, D. H. &; Wiesel, T. N. (1972) Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421–450.
KisvÁrday, Z. F., Martin, K. A. C., Freund, T. F., MaglÓczky, Z. S., Whitteridge, D. &; Somogyi, P. (1986) Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex. Experimental Brain Research 64, 541–552.
KisvÁrday, Z. F., Martin, K. A. C., Friedlander, M. J. &; Somogyi, P. (1987) Evidence for interlaminar inhibitory circuits in striate cortex of cat. Journal of Comparative Neurology 260, 1–19.
KisvÁrday, Z. F., Martin, K. A. C., Whitteridge, D. &; Somogyi, P. (1985) Synaptic connections of intracellularly filled clutch neurons: A type of small basket neuron in the visual cortex of the cat. Journal of Comparative Neurology 241, 111–137.
Kozloski, J., Hamzei-Sichani, F. &; Yuste, R. (2001) Stereotyped position of local synaptic targets in neocortex. Science 293, 868–872.
Levay, S. (1986) Synaptic organisation of claustral and geniculate afferents to the visual cortex of the cat. Journal of Neuroscience 6, 3564–3575.
Lorente de NÓ, R. (1949) Cerebral cortex: Architecture, intracortical connections, motor projections. In Physiology of the Nervous System (edited by Fulton, J.) pp. 288–313. New York: Oxford University Press.
Maletic-Savatic, M., Malinow, R. &; Svoboda, K. (1999) Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923–1927.
Martin, K. A. C. &; Whitteridge, D. (1984) Form, function and intracortical projections of neurones in the striate visual cortex of the cat. Journal of Physiology (London) 353, 463–504.
McGuire, B. A., Hornung, J. P., Gilbert, C. &; Wiesel, T. N. (1984) Patterns of synaptic input to layer 4 of cat striate cortex. Journal of Neuroscience 4, 3021–3033.
Mitchison, G. (1991) Neuronal branching patterns and the economy of cortical wiring. Proceedings of the Royal Society of London. Series B. Biological sciences 245, 151–158.
Muller, W. &; Connor, J. A. (1991) Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses. Nature 354, 73–76.
Peters, A. &; Kaiserman-Abramof, I. R. (1970) The small pyramidal neuron of the rat cerebral cortex. the perikaryon, dendrites and spines. American Journal of Anatomy 127, 321–356.
Press, W. H., Teukolsky, S. A., Vetterling, W. T. &; Flannery, B. P. (1997) Numerical Recipes in C. Cambridge: Cambridge University Press.
Reid, R. C. &; Alonso, J. M. (1995) Specificity of monosynaptic connections fromthalamus to visual cortex. Nature 378, 281–284.
Rockel, A. J., Hiorns, R. W. &; Powell, T. P. S. (1980) The basic uniformity in structure of the neocortex. Brain 103, 221–244.
Rockland, K. S. &; Knutson, T. (2001) Axon collaterals of Meynert cells diverge over large portions of area V1 in the macaque monkey. Journal of Comparative Neurology 441, 134–147.
Sholl, D. A. (1956) The Organization of the Cerebral Cortex. London: Methuen.
Silberberg, G., Gupta, A. &; Markram, H. (2002) Stereotypy in neocortical microcircuits. Trends in Neurosciences 25, 227–230.
Somogyi, P. (1989) Synaptic organization of GABAergic neurons and GABAa receptors in the lateral geniculate nucleus and visual cortex. In Neural Mechanisms of Visual Perception (edited by Lam, D. K. &; Gilbert, C. D.) pp. 35–62. Portfolio Publishing.
Somogyi, P. &; Cowey, A. (1981) Combined Golgi and electron microscopy study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey. Journal of Comparative Neurology 195, 547–566.
Somogyi, P., KisvÁrday, Z. F., Martin, K. A. C. &; Whitteridge, D. (1983) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of the cat. Neuroscience 10, 261–294.
Somogyi, P., TÁmas, G., Lujan, R. &; Buhl, E. H. (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Research. Brain Research Reviews 26, 113–135.
Strahler, A. N. (1957) Quantitative analysis of watershed geomorphology. Transactions of the American Geophysical Union 38, 913–920.
Swindale, N. V. (1981) Dendritic spines only connect. Trends in Neurosciences 4, 240–241.
SzentÁgothai, J. (1975) The 'module-concept' in cerebral cortex architecture. Brain Research 95, 475–496.
TamÁs, G., Buhl, E. H. &; Somogyi, P. (1997) Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurones in the cat visual cortex. Journal of Physiology (London) 500, 715–738.
TamÁs, G., Somogyi, P. &; Buhl, E. H. (1998) Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. Journal of Neuroscience 18, 4255–4270.
Tanaka, K. (1983) Cross-correlation analysis of geniculostriate neuronal relationships in cats. Journal of Neurophysiology 49, 1303–1318.
Tettoni, L., Gheorghita-Baechler, F., Bressoud, R., Welker, E. &; Innocenti, G. M. (1998) Constant and variable aspects of axonal phenotype in cerebral cortex. Cerebral Cortex 8, 543–552.
White, E. L. (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex. Structure, Function, and Theory. Boston, Basel: Birkhäuser.
Winfield, D. A. &; Powell, T. P. (1983) Laminar cell counts and geniculo-cortical boutons in area 17 of cat and monkey. Brain Research 277, 223–229.
Winfield, D. A., Rivera-Dominguez, M. &; Powell, T. P. S. (1981) The number and distribution of Meynert cells in area 17 of the macaque monkey. Proceedings of the Royal Society of London. Series B. Biological Sciences 213, 27–40.
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Anderson, J.C., Binzegger, T., Douglas, R.J. et al. Chance or design? Some specific considerations concerning synaptic boutons in cat visual cortex. J Neurocytol 31, 211–229 (2002). https://doi.org/10.1023/A:1024113707630
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DOI: https://doi.org/10.1023/A:1024113707630