Abstract
The total length of cortical axons could be reduced if the parent axons maintained straight trajectories and simply connected to dendritic shafts via spine-like terminaux boutons and to dendritic spines via bead-like en passant boutons. Cortical axons from cat area 17 were reconstructed from serial electron micrographs and their bouton morphology was correlated with their synaptic targets. En passant or terminaux boutons did not differ in the proportion of synapses they formed with dendritic spines and shafts, and thus, the two morphological variants of synaptic bouton do not contribute directly to optimizing axon length.
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References
Braitenberg, V. & Schüz, A. Anatomy of the Cortex (Springer, Berlin, 1991).
Peters, A. & Kaiserman-Abramof, I. R. Am. J. Anat. 127, 321–356 (1970).
Swindale, N. V. Trends Neurosci. 4, 240–241 (1981).
Gray, E. G. Trends Neurosci. 5, 5–6 (1982).
Fischer, M., Kaech, S., Knutti, D. & Matus, A. Neuron 20, 847–854 (1998).
Engert, F. & Bonhoeffer, T. Nature 399, 66–70 (1999).
Maletic-Savatic, M., Malinow, R. & Svoboda, K. Science 283, 1923–1927 (1999).
Toni, N., Buchs, P.-A., Nikonenko, I., Bron, C. R. & Muller, D. Nature 402, 421–425 (1999).
McGuire, B. A., Hornung, J.-P., Gilbert, C. D. & Wiesel, T. N. J. Neurosci. 4, 3021–3033 (1984).
Martin, K. A. C. & Whitteridge, D. J. Physiol. (Lond.) 353, 463–504 (1984).
Muller, W. & Connor, J. A. Nature 354, 73–76 (1991).
Guthrie, P. B., Segal, M. & Kater, S. B. Nature 354, 76–80 (1991).
Majewska, A., Tashiro, A. & Yuste, R. J. Neurosci. 20, 8262–8268 (2000).
Tarczy-Hornoch, K., Martin, K. A. C. & Stratford, K. J. Cereb. Cortex 9, 833–843 (1999).
Acknowledgements
We thank T. Binzegger for help with calculations and reconstructions. Additional support from EU (QULG3-1999-01064) and HFSP (RG0123/2000-B) grants to K.A.C.M.
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Supplementary Figure 1
Three-dimensional reconstruction from serial ultrathin sections of a labeled spiny stellate axon showing boutons and their targets in layer 2/3 of area 17 in cat visual cortex. (a) The radially aligned axon (blue) provides six bouton terminaux and two bouton en passant. The boutons terminaux and a single bouton en passant form a cluster and are centrally located. The second bouton terminaux is located at the uppermost end of the reconstruction. Three of the boutons formed synapses with dendritic shafts (light red) of which two formed numerous other asymmetric synapses (yellow) with unidentified boutons. The remaining boutons terminaux and bouton en passant formed synapses with spines (light brown/orange). (b) Detail of the central portion of the reconstruction seen in (a). The slender necks of the boutons terminaux are more clearly visible at this magnification. Color code as in (a). Scale bar, 2 μm. (PDF 634 kb)
Supplementary Figure 2
Reconstructions of labeled boutons in layer 2/3 from spiny stellate and pyramidal neurons in cat visual cortex. (a) A bouton terminaux (transparent blue) from a layer 3 pyramidal neuron forms a synapse with a spine (brown) that can be traced back to the parent dendrite (gray). Adjacent to the contacted spine is a second spine (brown) forming a complex asymmetric synapse with puncta adherens (all shown in yellow). (b) A small bouton terminaux (blue) from a layer 3 pyramidal neuron forms a synapse (yellow) with a dendritic shaft (transparent gray). The parent axon is in contact with the dendrite (lower right) and passes orthogonal to it but projects a short (~0.5 μm) bouton terminaux to form a synapse. (c) Two closely spaced (~2 μm) bouton en passant (transparent blue) from a spiny stellate neuron form synapses (yellow) with spines (transparent brown). Both boutons appear as swellings on the axon however the synapse of the lower bouton is formed on the surface that is projected away from the path of the axon. The synapse on the uppermost bouton is formed on the surface that is closest to the path of the axon and the swelling, which contains the synaptic vesicles and mitochondria, projects away from the synapse. (d) A bouton terminaux (blue) from a spiny stellate neuron forms a perforated synapse (yellow) with a spine (transparent brown). The spine lies on the path of, and is in contact with, the axon. But the synapse is formed by the bouton passing around a myelinated axon (transparent purple) and coming back to meet the path of the axon. The bouton lies adjacent both to the axon and the spine. Axes, 0.5 μm. (PDF 1527 kb)
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Anderson, J., Martin, K. Does bouton morphology optimize axon length?. Nat Neurosci 4, 1166–1167 (2001). https://doi.org/10.1038/nn772
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DOI: https://doi.org/10.1038/nn772
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