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Control of visually guided behavior by distinct populations of spinal projection neurons

Nature Neuroscience volume 11, pages 327–333 (2008)Cite this article

Abstract

A basic question in the field of motor control is how different actions are represented by activity in spinal projection neurons. We used a new behavioral assay to identify visual stimuli that specifically drive basic motor patterns in zebrafish. These stimuli evoked consistent patterns of neural activity in the neurons projecting to the spinal cord, which we could map throughout the entire population using in vivo two-photon calcium imaging. We found that stimuli that drive distinct behaviors activated distinct subsets of projection neurons, consisting, in some cases, of just a few cells. This stands in contrast to the distributed activation seen for more complex behaviors. Furthermore, targeted cell by cell ablations of the neurons associated with evoked turns abolished the corresponding behavioral response. This description of the functional organization of the zebrafish motor system provides a framework for identifying the complete circuit underlying a vertebrate behavior.

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Figure 1: Behavioral responses to drifting gratings.
Figure 2: Measuring calcium responses in spinal projection neurons.
Figure 3: Summary of direction tuning of all spinal projection neurons.
Figure 4: Spatial distribution of visually responsive cells.
Figure 5: Laser ablation of turning-selective neurons.

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Acknowledgements

The authors would like to thank M. Meister, T. Bonhoeffer, J.R. Sanes, B.P. Olveczky, M.C. Smear and J.E. Dowling for valuable comments on the manuscript, D.M. O'Malley for advice on experimental techniques, A.F. Schier for generous help with fish rearing and O.C. Orger for assistance with data analysis. This work was supported by postdoctoral fellowships from the Helen Hay Whitney Foundation (M.B.O.) and Human Frontier Science Program (J.H.B.), and US National Institutes of Health grant R01 EY014429-01A2 and funding from the McKnight and Dana Foundations (F.E.).

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Author notes

  1. Michael B Orger and Adam R Kampff: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, 02138, Massachusetts, USA

    Michael B Orger, Adam R Kampff, Johann H Bollmann & Florian Engert

  2. Department of Biology, Northeastern University, 360 Huntington Avenue, Boston, 02115, Massachusetts, USA

    Kristen E Severi

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  1. Michael B Orger
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Correspondence to Michael B Orger.

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Supplementary Text and Figures

Supplementary Figures 1–4 (PDF 243 kb)

Supplementary Movie 1

Phenotype of Mauthner array ablation. The left Mauthner cell and its segmental homologs have been ablated in a 6-d-old zebrafish. In response to a pressure pulse delivered by a picospritzer to the right of the body, the fish responds with a leftward tail bend with a latency of 8 ms. In contrast, the rightward bend elicited by the same stimulus delivered to the left side of the body has a latency of 35 ms. Flashed rectangle indicates the onset of the pulse. (AVI 4691 kb)

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Orger, M., Kampff, A., Severi, K. et al. Control of visually guided behavior by distinct populations of spinal projection neurons. Nat Neurosci 11, 327–333 (2008). https://doi.org/10.1038/nn2048

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