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The development of direction selectivity in ferret visual cortex requires early visual experience

Abstract

Development of the selective response properties that define columns in sensory cortex is thought to begin early in cortical maturation, without the need for experience. We investigated the development of direction selectivity in ferret visual cortex using optical imaging and electrophysiological techniques and found an exception to this view. Unlike orientation selectivity and ocular dominance, direction selectivity was not detected at eye opening. Direction selectivity emerged several days later and strengthened to adult levels over the following 2 weeks. Visual experience was essential for this process, as shown by the absence of direction selectivity in dark-reared ferrets. The impairment persisted in dark-reared ferrets that were given experience after this period, despite the recovery of response amplitude, preference and bandwidth for stimulus orientation, spatial and temporal frequency, and contrast. Visual experience in early postnatal life plays a necessary and unique role in the development of cortical direction selectivity.

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Figure 1: Development of direction and orientation selectivity.
Figure 2: Impaired development of direction selectivity in dark-reared ferrets.
Figure 3: Early visual experience promotes the development of direction selectivity.
Figure 4: Effects of varying spatial and temporal frequency and contrast.

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Acknowledgements

We thank T. Tucker and E. Johnson for assistance with analysis of optical imaging data, A. Basole for help with data collection, and members of the Fitzpatrick lab for critical comments. This work was supported by grants from the Whitehall Foundation to L.E.W. and the US National Institutes of Health to D.F.

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Correspondence to Leonard E White.

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Supplementary information

Supplementary Fig. 1

Ocular dominance in light-reared and dark-reared juvenile ferrets revealed by intrinsic signal optical imaging. (PDF 797 kb)

Supplementary Fig. 2

Orientation and direction selectivity signal in light-reared and dark-reared juvenile ferrets. (PDF 1533 kb)

Supplementary Fig. 3

Tuning of single unit recordings from layer 2/3 of V1 in dark-reared juvenile ferrets. (PDF 45 kb)

Supplementary Fig. 4

The effects of varying spatial and temporal frequency and stimulus contrast on orientation selectivity in juvenile ferrets reared under different conditions of visual experience. (PDF 1566 kb)

Supplementary Table 1

Direction selectivity of multi-unit recordings from layer 2/3 of V1 in light-reared and dark-reared juvenile ferrets. (PDF 45 kb)

Supplementary Table 2

Spatial and temporal frequency tuning and contrast sensitivity in V1 of light-reared and dark-reared juvenile ferrets and in dark-reared ferrets that were given late visual experience. (PDF 63 kb)

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Li, Y., Fitzpatrick, D. & White, L. The development of direction selectivity in ferret visual cortex requires early visual experience. Nat Neurosci 9, 676–681 (2006). https://doi.org/10.1038/nn1684

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