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The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex

Abstract

Sensory experience begins when neural circuits in the cerebral cortex are still immature; however, the contribution of experience to cortical maturation remains unclear. In the visual cortex, the selectivity of neurons for oriented stimuli at the time of eye opening is poor1,2,3,4,5 and increases dramatically after the onset of visual experience3,4,5,6,7,8. Here we investigate whether visual experience has a significant role in the maturation of orientation selectivity and underlying cortical circuits9,10,11,12 using two forms of deprivation: dark rearing, which completely eliminates experience, and binocular lid suture, which alters the pattern of sensory driven activity13. Orientation maps were present in dark-reared ferrets, but fully mature levels of tuning were never attained. In contrast, only rudimentary levels of orientation selectivity were observed in lid-sutured ferrets. Despite these differences, horizontal connections in both groups were less extensive and less clustered than normal, suggesting that long-range cortical processing is not essential for the expression of orientation selectivity, but may be needed for the full maturation of tuning. Thus, experience is beneficial or highly detrimental to cortical maturation, depending on the pattern of sensory driven activity.

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Figure 1: Maps of orientation preference in normal and visually deprived ferrets.
Figure 2: Quantitative assessment of orientation preference in normal and visually deprived ferrets.
Figure 3: Horizontal connections in layer 2/3 of normal and visually deprived ferrets.

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Acknowledgements

We thank B. Bosking and J. Crowley for discussions.

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Correspondence to Leonard E. White.

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White, L., Coppola, D. & Fitzpatrick, D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 411, 1049–1052 (2001). https://doi.org/10.1038/35082568

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