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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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  1. Henry, G. H., Bishop, P. O., Tupper, R. M. & Dreher, B. Orientation specificity and response variability of cells in striate cortex. Vision Res. 13, 1771–1779 (1973)

    Article  CAS  Google Scholar 

  2. Schiller, P. H., Finlay, B. L. & Volman, S. F. Short-term response variability of monkey striate neurons. Brain Res. 105, 347–349 (1976)

    Article  CAS  Google Scholar 

  3. Vogels, R., Spileers, W. & Orban, G. A. The response variability of striate cortical neurons in the behaving monkey. Exp. Brain Res. 77, 432–436 (1989)

    Article  CAS  Google Scholar 

  4. Azouz, R. & Gray, C. M. Cellular mechanisms contributing to response variability of cortical neurons in vivo. J. Neurosci. 19, 2209–2223 (1999)

    Article  CAS  Google Scholar 

  5. Zohary, E., Shadlen, M. N. & Newsome, W. T. Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370, 140–143 (1994)

    Article  ADS  CAS  Google Scholar 

  6. Shadlen, M. N. & Newsome, W. T. The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870–3896 (1998)

    Article  CAS  Google Scholar 

  7. Pouget, A., Dayan, P. & Zemel, R. Inference and computation with population codes. Annu. Rev. Neurosci. 26, 381–410 (2004)

    Article  Google Scholar 

  8. Meister, M., Wong, R. O. L., Baylor, D. A. & Shatz, C. J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943 (1991)

    Article  ADS  CAS  Google Scholar 

  9. Arieli, A., Shoham, D., Hildesheim, R. & Grinvald, A. Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. J. Neurophysiol. 73, 2072–2093 (1995)

    Article  CAS  Google Scholar 

  10. Weliky, M. & Katz, L. C. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 285, 599–604 (1999)

    Article  CAS  Google Scholar 

  11. Tsodyks, M., Kenet, T., Grinvald, A. & Arieli, A. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286, 1943–1946 (1999)

    Article  CAS  Google Scholar 

  12. Chiu, C. & Weliky, M. Spontaneous activity in developing ferret visual cortex in vivo. J. Neurosci. 21, 8906–8914 (2001)

    Article  CAS  Google Scholar 

  13. Kenet, T., Bibitchkov, D., Tsodyks, M., Grinvald, A. & Arieli, A. Spontaneously emerging cortical representations of visual attributes. Nature 425, 954–956 (2003)

    Article  ADS  CAS  Google Scholar 

  14. Gao, W., Newman, D. E., Wormington, A. B. & Pallas, S. Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: Immunocytochemical localization of GABAergic neurons. J. Comp. Neurol. 409, 261–273 (1999)

    Article  CAS  Google Scholar 

  15. Anderson, J., Lampl, I., Reichova, I., Carandini, M. & Ferster, D. Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex. Nature Neurosci. 3, 617–621 (2000)

    Article  CAS  Google Scholar 

  16. Cossart, R., Aronov, D. & Yuste, R. Attractor dynamics of network UP states in the neocortex. Nature 423, 283–288 (2003)

    Article  ADS  CAS  Google Scholar 

  17. Shu, Y. S., Hasenstaub, A., Badoual, M., Bal, T. & McCormick, D. A. Barrages of synaptic activity control the gain and sensitivity of cortical neurons. J. Neurosci. 23, 10388–10401 (2003)

    Article  CAS  Google Scholar 

  18. Gallant, J. L., Connor, C. E. & Van Essen, D. C. Neural activity in areas V1, V2 and V4 during free viewing of natural scenes compared to controlled viewing. Neuroreport 9, 1673–1678 (1998)

    Article  CAS  Google Scholar 

  19. Vinje, W. E. & Gallant, J. L. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273–1276 (2000)

    Article  ADS  CAS  Google Scholar 

  20. Gawne, T. J. & Richmond, B. J. How independent are the messages carried by adjacent inferior temporal cortical neurons? J. Neurosci. 13, 2758–2771 (1993)

    Article  CAS  Google Scholar 

  21. Pola, G., Thiele, A., Hoffmann, K. P. & Panzeri, S. An exact method to quantify the information transmitted by different mechanisms of correlational coding. Network Comput. Neural Syst. 14, 35–60 (2003)

    Article  CAS  Google Scholar 

  22. Nirenberg, S. & Latham, P. E. Decoding neuronal spike trains: How important are correlations? Proc Natl Acad. Sci. USA 100, 1045–1050 (2003)

    Article  Google Scholar 

  23. Kara, P., Reinagel, P. & Reid, R. C. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27, 635–646 (2000)

    Article  CAS  Google Scholar 

  24. Hirsch, J. A. et al. Synaptic physiology of the flow of information in the cat's visual cortex in vivo. J. Physiol. (Lond.) 540, 335–350 (2002)

    Article  CAS  Google Scholar 

  25. Attwell, D. & Laughlin, S. B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 21, 1133–1145 (2001)

    Article  CAS  Google Scholar 

  26. Lennie, P. The cost of cortical computation. Curr. Biol. 13, 493–497 (2003)

    Article  CAS  Google Scholar 

  27. Weliky, M., Fiser, J., Hunt, R. H. & Wagner, D. N. Coding of natural scenes in primary visual cortex. Neuron 37, 703–718 (2003)

    Article  CAS  Google Scholar 

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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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