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Small modulation of ongoing cortical dynamics by sensory input during natural vision


During vision, it is believed that neural activity in the primary visual cortex is predominantly driven by sensory input from the environment. However, visual cortical neurons respond to repeated presentations of the same stimulus with a high degree of variability1,2,3,4. Although this variability has been considered to be noise owing to random spontaneous activity within the cortex5,6,7, recent studies show that spontaneous activity has a highly coherent spatio-temporal structure8,9,10,11,12,13. This raises the possibility that the pattern of this spontaneous activity may shape neural responses during natural viewing conditions to a larger extent than previously thought. Here, we examine the relationship between spontaneous activity and the response of primary visual cortical neurons to dynamic natural-scene and random-noise film images in awake, freely viewing ferrets from the time of eye opening to maturity. The correspondence between evoked neural activity and the structure of the input signal was weak in young animals, but systematically improved with age. This improvement was linked to a shift in the dynamics of spontaneous activity. At all ages including the mature animal, correlations in spontaneous neural firing were only slightly modified by visual stimulation, irrespective of the sensory input. These results suggest that in both the developing and mature visual cortex, sensory evoked neural activity represents the modulation and triggering of ongoing circuit dynamics by input signals, rather than directly reflecting the structure of the input signal itself.

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Figure 1: Statistical properties of natural-scene and random-noise film images.
Figure 2: Time series plots of neural activity recorded under the three interleaved stimulus conditions at three different ages.
Figure 3: Developmental changes in the spatio-temporal pattern of stimulus-evoked and spontaneous visual cortical activity in awake-behaving ferrets.
Figure 4: Developmental changes in the spatio-temporal pattern of stimulus-evoked and spontaneous visual cortical activity in anaesthetized ferrets.

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This work was supported by NIH (NEI) and the McKnight Foundation. We thank David Wagner for technical assistance. We also thank R. Aslin, D. Knill, D. Lee and K. Nordeen for comments. We also thank E. Romanski for supplying the ISCAN equipment.

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Correspondence to Michael Weliky.

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Supplementary Data

This file contains three sections. S1 offers a brief discussion of the individual pair-wise cross-correlation analysis. A figure and the corresponding figure legend are provided. In S2, details of eye-movement monitoring are supplied. We included a paragraph on methods, a figure and the figure legend. The final section, S3, contains a figure and its figure legend regarding the recordings under anaesthesia. Two references are provided at the end. (PDF 220 kb)

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Fiser, J., Chiu, C. & Weliky, M. Small modulation of ongoing cortical dynamics by sensory input during natural vision. Nature 431, 573–578 (2004).

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