Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex

Abstract

Membrane potentials of cortical neurons fluctuate between a hyperpolarized (‘down’) state and a depolarized (‘up’) state which may be separated by up to 30 mV, reflecting rapid but infrequent transitions between two patterns of synaptic input. Here we show that such fluctuations may contribute to representation of visual stimuli by cortical cells. In complex cells of anesthetized cats, where such fluctuations are most prominent, prolonged visual stimulation increased the probability of the up state. This probability increase was related to stimulus strength: its dependence on stimulus orientation and contrast matched each cell's averaged membrane potential. Thus large fluctuations in membrane potential are not simply noise on which visual responses are superimposed, but may provide a substrate for encoding sensory information.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Responses of a complex cell to a drifting grating of optimal orientation and spatial frequency.
Figure 2: Prevalence of two-state fluctuations in simple and complex cells.
Figure 3: Visual responses of complex cells.
Figure 4: Visual response properties derived from membrane potential fluctuations in complex cells.
Figure 5: Contribution of membrane potential fluctuations to changes in firing rate during the up state.

Similar content being viewed by others

References

  1. Carandini, M. & Ferster, D. A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276, 949–952 (1997).

    Article  CAS  Google Scholar 

  2. Lampl, I., Reichova, I. & Ferster, D. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22, 361–374 (1999).

    Article  CAS  Google Scholar 

  3. Wilson, C. J. & Groves, P. M. Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res. 220, 67–80 (1981).

    Article  CAS  Google Scholar 

  4. Wilson, C. J. The generation of natural firing patterns in neostriatal neurons. Prog. Brain Res. 99, 277–297 (1993).

    Article  CAS  Google Scholar 

  5. Wilson, C. J. & Kawaguchi, Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci. 16, 2397–2410 (1996).

    Article  CAS  Google Scholar 

  6. Stern, E. A., Kincaid, A. E. & Wilson, C. J. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J. Neurophysiol. 77, 1697–1715 (1997).

    Article  CAS  Google Scholar 

  7. Plenz, D. & Kitai, S. T. Up and down states in striatal medium spiny neurons simultaneously recorded with spontaneous activity in fast-spiking interneurons studied in cortex-striatum-substantia nigra organotypic cultures. J. Neurosci. 18, 266–283 (1998).

    Article  CAS  Google Scholar 

  8. Stern, E. A., Jaeger, D. & Wilson, C. J. Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo. Nature 394, 475–478 (1998).

    Article  CAS  Google Scholar 

  9. Steriade, M., Contreras, D., Curro Dossi, R. & Nunez, A. The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J. Neurosci. 13, 3284–3299 (1993).

    Article  CAS  Google Scholar 

  10. Metherate, R. & Ashe, J. H. Ionic flux contributions to neocortical slow waves and nucleus basalis-mediated activation: whole-cell recordings in vivo. J. Neurosci. 13, 5312–5323 (1993).

    Article  CAS  Google Scholar 

  11. Arieli, A., Sterkin, A., Grinvald, A. & Aertsen, A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273, 1868–1871 (1996).

    Article  CAS  Google Scholar 

  12. Stevens, C. F. & Zador, A. M. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1, 210–217 (1998).

    Article  CAS  Google Scholar 

  13. Movshon, J. A., Thompson, I. D. & Tolhurst, D. J. Receptive field organization of complex cells in the cat's striate cortex. J. Physiol. (Lond.) 283, 79–99 (1978).

    Article  CAS  Google Scholar 

  14. Skottun, B. C. et al. Classifying simple and complex cells on the basis of response modulation. Vision Res. 31, 1079–1086 (1991).

    CAS  PubMed  Google Scholar 

  15. Jagadeesh, B., Gray, C. M. & Ferster, D. Visually evoked oscillations of membrane potential in cells of cat visual cortex. Science 257, 552–554 (1992).

    Article  CAS  Google Scholar 

  16. Gustafsson, B. & McCrea, D. Influence of stretch-evoked synaptic potentials on firing probability of cat spinal motoneurones. J. Physiol. (Lond.) 347, 431–451 (1984).

    Article  CAS  Google Scholar 

  17. Mainen, Z. F. & Sejnowski, T. J. Reliability of spike timing in neocortical neurons. Science 268, 1503–1506 (1995).

    Article  CAS  Google Scholar 

  18. 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 

  19. Carandini, M. & Ferster, D. Orientation tuning of membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20, 470–484 (2000).

    Article  CAS  Google Scholar 

  20. Metherate, R., Cox, C. L. & Ashe, J. H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J. Neurosci. 12, 4701–4711 (1992).

    Article  CAS  Google Scholar 

  21. Gray, C. M., Konig, P., Engel, A. K. & Singer, W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337 (1989).

    Article  CAS  Google Scholar 

  22. Gilbert, C. D. Laminar differences in receptive properties of cells in cat primary visual cortex. J. Physiol. (Lond.) 268, 391–421 (1977).

    Article  CAS  Google Scholar 

  23. Douglas, R. J. & Martin, K. A. A functional microcircuit for cat visual cortex. J. Physiol. (Lond.) 440, 735–769 (1991).

    Article  CAS  Google Scholar 

  24. Ben-Yishai, R., Or, R. L. B. & Sompolinsky, H. Theory of orientation tuning in the visual cortex. Proc. Natl. Acad. Sci. USA 92, 3844–3848 (1995).

    Article  CAS  Google Scholar 

  25. Somers, D. C., Nelson, S. B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448–5465 (1995).

    Article  CAS  Google Scholar 

  26. Douglas, R. J., Martin, K. A. C. & Whitteridge, D. An intracellular analysis of the visual responses of neurones in cat visual cortex. J. Physiol. (Lond.) 440, 659–696 (1991).

    Article  CAS  Google Scholar 

  27. Steriade, M., Nunez, A. & Amzica, F. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13, 3252–3265 (1993).

    Article  CAS  Google Scholar 

  28. Steriade, M., Nunez, A. & Amzica, F. Intracellular analysis of the relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 13, 3266–3283 (1993).

    Article  CAS  Google Scholar 

  29. 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 

  30. Chung, S. & Ferster, D. Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron 20, 1177–1189 (1998).

    Article  CAS  Google Scholar 

  31. Blanton, M. G., Lo Turco, J. J. & Kriegstein, A. R. Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J. Neurosci. Methods 30, (1989).

  32. Neher, E. in Methods in Enzymology: Ion Channels (eds. Rudy, B. & Iverson, L. E.) 123–131 (Academic, New York, 1992).

    Book  Google Scholar 

Download references

Acknowledgements

This work was supported by an NIH grant (R01EY04726). J.A. was supported by a NEI training grant (P32EY07128). We thank Indira Raman, Deda Gillespie, Michael Stryker and Nelson Spruston for comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Ferster.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anderson, J., Lampl, I., Reichova, I. et al. Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex. Nat Neurosci 3, 617–621 (2000). https://doi.org/10.1038/75797

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/75797

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing