Emergence of binocular functional properties in a monocular neural circuit

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Abstract

Sensory circuits frequently integrate converging inputs while maintaining precise functional relationships between them. For example, in mammals with stereopsis, neurons at the first stages of binocular visual processing show a close alignment of receptive-field properties for each eye. Still, basic questions about the global wiring mechanisms that enable this functional alignment remain unanswered, including whether the addition of a second retinal input to an otherwise monocular neural circuit is sufficient for the emergence of these binocular properties. We addressed this question by inducing a de novo binocular retinal projection to the larval zebrafish optic tectum and examining recipient neuronal populations using in vivo two-photon calcium imaging. Notably, neurons in rewired tecta were predominantly binocular and showed matching direction selectivity for each eye. We found that a model based on local inhibitory circuitry that computes direction selectivity using the topographic structure of both retinal inputs can account for the emergence of this binocular feature.

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Figure 1: Functional analysis of the rewired larval zebrafish retinotectal circuit.
Figure 2: Binocular functional integration in rewired tecta.
Figure 3: Tectal populations show equivalent functional retinotopy for each eye.
Figure 4: Binocular neurons show matching direction selectivity for each eye.
Figure 5: Tectal neurons show sequence selectivity to binocular apparent motion.
Figure 6: Tectal direction selectivity requires local inhibition.

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Acknowledgements

We extend our gratitude to A. Kampff for help in microscope construction, J. Bollmann for a suggestion on microscope optimization and M. Orger for insightful discussions. The authors thank M. Livingstone, M. Meister, T. Bonhoeffer, J. Lichtman, V. Murthy, A. Schier, B. Olvecsky and members of the Engert laboratory for comments on the manuscript and helpful discussions. This work was supported by a National Science Foundation Predoctoral Fellowship, a National Science and Engineering Graduate Fellowship (P.R.), a US National Institutes of Health grant (R01 EY014429-01A2) and funding from the McKnight and Dana Foundations (F.E.).

Author information

P.R. carried out the experiments and analyzed the data. P.R. and F.E. designed the experiments and wrote the manuscript.

Correspondence to Florian Engert.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–3 (PDF 1696 kb)

Supplementary Video 1

Calcium imaging of binocular visually driven tectal population activity in a rewired larval zebrafish. Tectal neurons respond to visual stimulation with 3° moving spots shown to either the ipsilateral (left) or the contralateral (right) eye. Stimuli are shown schematically in the lower left corner. (AVI 32038 kb)

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Ramdya, P., Engert, F. Emergence of binocular functional properties in a monocular neural circuit. Nat Neurosci 11, 1083–1090 (2008) doi:10.1038/nn.2166

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