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Experience with moving visual stimuli drives the early development of cortical direction selectivity

Abstract

The onset of vision occurs when neural circuits in the visual cortex are immature, lacking both the full complement of connections1,2 and the response selectivity that defines functional maturity3,4. Direction-selective responses are particularly vulnerable to the effects of early visual deprivation, but it remains unclear how stimulus-driven neural activity guides the emergence of cortical direction selectivity. Here we report observations from a motion training protocol that allowed us to monitor the impact of experience on the development of direction-selective responses in visually naive ferrets. Using intrinsic signal imaging techniques, we found that training with a single axis of motion induced the rapid emergence of direction columns that were confined to cortical regions preferentially activated by the training stimulus. Using two-photon calcium imaging techniques, we found that single neurons in visually naive animals exhibited weak directional biases and lacked the strong local coherence in the spatial organization of direction preference that was evident in mature animals. Training with a moving stimulus, but not with a flashed stimulus, strengthened the direction-selective responses of individual neurons and preferentially reversed the direction biases of neurons that deviated from their neighbours. Both effects contributed to an increase in local coherence. We conclude that early experience with moving visual stimuli drives the rapid emergence of direction-selective responses in the visual cortex.

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Figure 1: Rapid emergence of direction columns with motion training.
Figure 2: Direction selectivity of cells in visually naive and experienced ferrets, demonstrated by two-photon calcium imaging.
Figure 3: Motion training increases direction selectivity in individual cells.
Figure 4: Impact of normal experience and motion training on direction preference.

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Acknowledgements

The authors thank P. Kara, T. Mrsic-Flogel and A. Kerlin for help with two-photon imaging techniques, T. Tucker and J. Heiner for technical assistance and M. Christensson and the members of the Fitzpatrick lab for comments on the manuscript. This work was supported by grants from the Whitehall Foundation to L.E.W. and the US National Institutes of Health to D.F. and S.D.V.H.

Author Contributions Y.L. performed intrinsic imaging experiments and analysis. Y.L. and S.D.V.H. performed two-photon experiments, and S.D.V.H., Y.L. and M.M. analyzed the two-photon data. Y.L., S.D.V.H., L.E.W. and D.F. wrote the paper, and all authors discussed the results and commented on the manuscript.

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Correspondence to David Fitzpatrick.

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Li, Y., Van Hooser, S., Mazurek, M. et al. Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456, 952–956 (2008). https://doi.org/10.1038/nature07417

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