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Heterogeneity in synaptic transmission along a Drosophila larval motor axon

Nature Neuroscience volume 8, pages 1188–1196 (2005)Cite this article

An Erratum to this article was published on 01 October 2005

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Abstract

At the Drosophila melanogaster larval neuromuscular junction (NMJ), a motor neuron releases glutamate from 30–100 boutons onto the muscle it innervates. How transmission strength is distributed among the boutons of the NMJ is unknown. To address this, we created synapcam, a version of the Ca2+ reporter Cameleon. Synapcam localizes to the postsynaptic terminal and selectively reports Ca2+ influx through glutamate receptors (GluRs) with single-impulse and single-bouton resolution. GluR-based Ca2+ signals were uniform within a given connection (that is, a given bouton/postsynaptic terminal pair) but differed considerably among connections of an NMJ. A steep gradient of transmission strength was observed along axonal branches, from weak proximal connections to strong distal ones. Presynaptic imaging showed a matching axonal gradient, with higher Ca2+ influx and exocytosis at distal boutons. The results suggest that transmission strength is mainly determined presynaptically at the level of individual boutons, possibly by one or more factors existing in a gradient.

*Note: In the version of this article initially published online, the second author’s name was misspelled. The correct spelling should be Dierk F Reiff. The error has been corrected in the HTML version of the article. This correction has been appended to the PDF and print versions.

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Figure 1: Synapcam expression has no affect on NMJ development or physiology.
Figure 2: Synapcams report Ca2+ flux through GluRs as an increase in FRET.
Figure 3: Synapcam reveals transmission heterogeneity at the Drosophila NMJ.
Figure 4: Synapcam3.1 is not saturated by single stimuli to the motor axon.
Figure 5: Prolonged imaging shows the distribution of transmission strength of an NMJ.
Figure 6: A proximal-distal gradient in transmission strength.
Figure 7: Presynaptic contribution to the gradient of transmission strength.

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  • 04 September 2005

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Acknowledgements

We thank D. Raymond for developing the Bouton Project software; K. Zito for initial cloning and transfection of synapcam3.1 and M.-M. Poo, R. Zucker and M. Neff for comments on the manuscript. This work was funded by a US National Institutes of Health grant (E.Y.I. and C.S.G.), the Max-Planck-Society (D.F.R. and A.B.) and the Howard Hughes Medical Institute (G.G. and C.S.G.).

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Author notes

  1. Corey S Goodman

    Present address: Renovis, Inc., Two Corporate Drive, South San Francisco, California, 94080, USA

Authors and Affiliations

  1. Department of Molecular and Cell Biology, 279 Life Sciences Addition, University of California Berkeley, Berkeley, 94720, California, USA

    Giovanna Guerrero, Corey S Goodman & Ehud Y Isacoff

  2. Department of Systems and Computational Neurobiology, Max-Planck-Institute of Neurobiology, Am Klopfersptiz 18 A, Martinsried, 82152, Germany

    Dierk F Reiff & Alexander Borst

  3. Helen Wills Neuroscience Institute, 279 Life Sciences Addition, University of California Berkeley, Berkeley, 94720, California, USA

    Gautam Agarwal, Robin W Ball, Corey S Goodman & Ehud Y Isacoff

  4. Physical Bioscience and Material Science Divisions, Lawrence Berkeley National Laboratory, Berkeley, 94720, California, USA

    Ehud Y Isacoff

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Supplementary information

Supplementary Fig. 1

The relative increase in ΔFRET or decrease in current after two stimuli is smaller for postsynaptic terminals and NMJs with higher transmission. (PDF 267 kb)

Supplementary Fig. 2

GluR identity and distribution cannot explain the proximal-distal gradient of transmission strength. (PDF 4397 kb)

Supplementary Fig. 3

Differences between boutons in the number of active zone patches or the total quantity of an active zone marker cannot explain the proximal-distal gradient of transmission strength. (PDF 340 kb)

Supplementary Fig. 4

Possible origins for a presynaptic gradient of transmission strength. (PDF 553 kb)

Supplementary Table 1

Recording conditions and synapcam3.1 expression do not affect the physiological properties of the NMJ. (PDF 77 kb)

Supplementary Methods (PDF 90 kb)

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Guerrero, G., Reiff, D., Agarwal, G. et al. Heterogeneity in synaptic transmission along a Drosophila larval motor axon. Nat Neurosci 8, 1188–1196 (2005). https://doi.org/10.1038/nn1526

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