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Development and spike timing–dependent plasticity of recurrent excitation in the Xenopus optic tectum

Nature Neuroscience volume 11, pages 467–475 (2008)Cite this article

Abstract

Much of the information processing in the brain occurs at the level of local circuits; however, the mechanisms underlying their initial development are poorly understood. We sought to examine the early development and plasticity of local excitatory circuits in the optic tectum of Xenopus laevis tadpoles. We found that retinal input recruits persistent, recurrent intratectal synaptic excitation that becomes more temporally compact and less variable over development, thus increasing the temporal coherence and precision of tectal cell spiking. We also saw that patterned retinal input can sculpt recurrent activity according to a spike timing–dependent plasticity rule, and that impairing this plasticity during development results in abnormal refinement of the temporal characteristics of recurrent circuits. This plasticity is a previously unknown mechanism by which patterned retinal activity allows intratectal circuitry to self-organize, optimizing the temporal response properties of the tectal network, and provides a substrate for rapid modulation of tectal neuron receptive-field properties.

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Figure 1: Developmental changes in temporal response properties of tectal neuron spiking.
Figure 2: Subthreshold synaptic responses underlying tectal cell spiking.
Figure 3: Developmental changes in recurrent excitation in the tectum.
Figure 4: Comparison of spontaneous and evoked sEPSCs over development.
Figure 5: STDP of recurrent excitatory network activity.
Figure 6: In vivo visual experience shapes temporal properties of recurrent excitation.
Figure 7: NMDA and Ca2+-permeable AMPARs are required for plasticity and the development of recurrent excitatory tectal circuitry.

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Acknowledgements

We thank I. Sears for technical support and D. Berson, M. Mehta, E. Bienenstock and members of the Aizenman lab for helpful discussion. K.G.P. is supported by an National Research Service Award from the US National Eye Institute, and C.D.A. is supported by a generous gift from the Klingenstein Foundation and the American Heart Association.

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Authors and Affiliations

  1. Department of Neuroscience, Brown University, Box G-LN, Providence, 02912, Rhode Island, USA

    Kara G Pratt, Wei Dong & Carlos D Aizenman

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  1. Kara G Pratt
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  2. Wei Dong
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  3. Carlos D Aizenman
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Contributions

K.G.P., W.D. and C.D.A. all contributed to the experimental design, electrophysiology experiments, data analysis and preparation of the figures. K.G.P. and C.D.A. also prepared the manuscript.

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Correspondence to Carlos D Aizenman.

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Pratt, K., Dong, W. & Aizenman, C. Development and spike timing–dependent plasticity of recurrent excitation in the Xenopus optic tectum. Nat Neurosci 11, 467–475 (2008). https://doi.org/10.1038/nn2076

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