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GABAergic circuits control stimulus-instructed receptive field development in the optic tectum

Nature Neuroscience volume 13, pages 1098–1106 (2010)Cite this article

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Abstract

During the development of sensory systems, receptive fields are modified by stimuli in the environment. This is thought to rely on learning algorithms that are sensitive to correlations in spike timing between cells, but the manner in which developing circuits selectively exploit correlations that are related to sensory inputs is unknown. We recorded from neurons in the developing optic tectum of Xenopus laevis and found that repeated presentation of moving visual stimuli induced receptive field changes that reflected the properties of the stimuli and that this form of learning was disrupted when GABAergic transmission was blocked. Consistent with a role for spike timing–dependent mechanisms, GABA blockade altered spike-timing patterns in the tectum and increased correlations between cells that would affect plasticity at intratectal synapses. This is a previously unknown role for GABAergic signals in development and highlights the importance of regulating the statistics of spiking activity for learning.

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Figure 1: Examining stimulus-driven receptive field changes in tectal neurons.
Figure 2: Moving stimuli instruct asymmetric changes in tectal receptive fields.
Figure 3: Blocking GABAergic inputs eliminates instructive training effects on tectal receptive fields.
Figure 4: Effects of GABAA receptor blockade on baseline receptive field properties.
Figure 5: GABA blockade boosts temporal correlations between tectal neurons during training.
Figure 6: Receptive field changes are altered by manipulations of spike timing during training.
Figure 7: GABAergic circuits reduce spatiotemporal correlations in tectal receptive fields.
Figure 8: The timing of synaptic inputs underlies GABAergic control of tectal spiking.

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Acknowledgements

We would like to thank H. Cline, K. Lamsa and O. Paulsen for helpful discussions and for comments on the manuscript. This work was supported by grants from the Biotechnology and Biological Sciences Research Council (BB/E0154761) and the Medical Research Council (G0601503). The research leading to these results has received funding from the European Research Council under the European Community's Seventh Framework Programme (FP7/2007-2013), ERC grant agreement number 243273. In addition, C.J.A. was supported by a Fellowship from the Research Councils UK and British Pharmacological Society, and B.A.R. was supported by a Wellcome Trust Doctoral Fellowship and a Post Graduate Scholarship from the Natural Sciences and Engineering Research Council of Canada.

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  1. Department of Pharmacology, Oxford University, Oxford, UK

    Blake A Richards, Oliver P Voss & Colin J Akerman

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  1. Blake A Richards
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B.A.R. conducted the experiments. B.A.R., O.P.V. and C.J.A. designed the experiments, contributed to the data analysis, prepared the figures and wrote the manuscript.

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Correspondence to Colin J Akerman.

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Richards, B., Voss, O. & Akerman, C. GABAergic circuits control stimulus-instructed receptive field development in the optic tectum. Nat Neurosci 13, 1098–1106 (2010). https://doi.org/10.1038/nn.2612

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