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 contrast modulates functional connectivity in visual cortex

Nature Neuroscience volume 12, pages 70–76 (2009)Cite this article

Abstract

Neurons in visual cortex are linked by an extensive network of lateral connections. To study the effect of these connections on neural responses, we recorded spikes and local field potentials (LFPs) from multi-electrode arrays that were implanted in monkey and cat primary visual cortex. Spikes at each location generated outward traveling LFP waves. When the visual stimulus was absent or had low contrast, these LFP waves had large amplitudes and traveled over long distances. Their effect was strong: LFP traces at any site could be predicted by the superposition of waves that were evoked by spiking in a ∼1.5-mm radius. As stimulus contrast increased, both the magnitude and the distance traveled by the waves progressively decreased. We conclude that the relative weight of feedforward and lateral inputs in visual cortex is not fixed, but rather depends on stimulus contrast. Lateral connections dominate at low contrast, when spatial integration of signals is perhaps most beneficial.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Spike-triggered LFPs as a measure of functional connectivity.
Figure 2: Spikes initiate traveling waves of LFPs in the cortex.
Figure 3: Predictions of LFPs from the spiking activity across a neuronal population.
Figure 4: Sites with similar orientation preference are more strongly linked than sites with dissimilar orientation preference.
Figure 5: Visual stimulation modifies the effective lateral connectivity in the cortex.
Figure 6: Effect of contrast on the magnitude and spatial extent of lateral interactions.
Figure 7: Results are unchanged by triggering on multi-unit or single-unit activity.
Figure 8: Correlation between pairs of LFP signals shows a contrast dependence that is similar to spike-triggered averaging of LFPs.

Similar content being viewed by others

References

  1. Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).

    Article  CAS  Google Scholar 

  2. Priebe, N.J. & Ferster, D. Inhibition, spike threshold and stimulus selectivity in primary visual cortex. Neuron 57, 482–497 (2008).

    Article  CAS  Google Scholar 

  3. Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252 (1996).

    Article  CAS  Google Scholar 

  4. Ferster, D. & Miller, K.D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441–471 (2000).

    Article  CAS  Google Scholar 

  5. 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 

  6. Ringach, D.L., Hawken, M.J. & Shapley, R. Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281–284 (1997).

    Article  CAS  Google Scholar 

  7. Sompolinsky, H. & Shapley, R. New perspectives on the mechanisms for orientation selectivity. Curr. Opin. Neurobiol. 7, 514–522 (1997).

    Article  CAS  Google Scholar 

  8. Bringuier, V., Chavane, F., Glaeser, L. & Fregnac, Y. Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283, 695–699 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. 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 

  11. Allman, J., Miezin, F. & McGuinness, E. Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. Annu. Rev. Neurosci. 8, 407–430 (1985).

    Article  CAS  Google Scholar 

  12. Levitt, J.B. & Lund, J.S. Contrast dependence of contextual effects in primate visual cortex. Nature 387, 73–76 (1997).

    Article  CAS  Google Scholar 

  13. Angelucci, A. et al. Circuits for local and global signal integration in primary visual cortex. J. Neurosci. 22, 8633–8646 (2002).

    Article  CAS  Google Scholar 

  14. Jin, J.Z. et al. On and off domains of geniculate afferents in cat primary visual cortex. Nat. Neurosci. 11, 88–94 (2008).

    Article  CAS  Google Scholar 

  15. Katzner, S. et al. Local origin of field potentials in visual cortex. Neuron (in the press).

  16. Kitano, M., Niiyama, K., Kasamatsu, T., Sutter, E.E. & Norcia, A.M. Retinotopic and nonretinotopic field potentials in cat visual cortex. Vis. Neurosci. 11, 953–977 (1994).

    Article  CAS  Google Scholar 

  17. Benucci, A., Frazor, R.A. & Carandini, M. Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron 55, 103–117 (2007).

    Article  CAS  Google Scholar 

  18. Grinvald, A., Lieke, E.E., Frostig, R.D. & Hildesheim, R. Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J. Neurosci. 14, 2545–2568 (1994).

    Article  CAS  Google Scholar 

  19. Gilbert, C.D. & Wiesel, T.N. Clustered intrinsic connections in cat visual cortex. J. Neurosci. 3, 1116–1133 (1983).

    Article  CAS  Google Scholar 

  20. Hirsch, J.A. & Gilbert, C.D. Synaptic physiology of horizontal connections in the cats' visual cortex. J. Neurosci. 11, 1800–1809 (1991).

    Article  CAS  Google Scholar 

  21. Bosking, W.H., Zhang, Y., Schofield, B. & Fitzpatrick, D. Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J. Neurosci. 17, 2112–2127 (1997).

    Article  CAS  Google Scholar 

  22. Nowak, L.G., Munk, M.H., James, A.C., Girard, P. & Bullier, J. Cross-correlation study of the temporal interactions between areas V1 and V2 of the macaque monkey. J. Neurophysiol. 81, 1057–1074 (1999).

    Article  CAS  Google Scholar 

  23. Song, S., Sjöström, P.J., Reigl, M., Nelson, S. & Chklovskii, D.B. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3, e68 (2005).

    Article  Google Scholar 

  24. de la Rocha, J., Doiron, B., Shea-Brown, E., Josic, K. & Reyes, A. Correlation between neural spike trains increases with firing rate. Nature 448, 802–806 (2007).

    Article  CAS  Google Scholar 

  25. Dorn, J.D. & Ringach, D.L. Estimating membrane voltage correlations from extracellular spike trains. J. Neurophysiol. 89, 2271–2278 (2003).

    Article  Google Scholar 

  26. Aertsen, A.M. & Gerstein, G.L. Evaluation of neuronal connectivity: sensitivity of cross-correlation. Brain Res. 340, 341–354 (1985).

    Article  CAS  Google Scholar 

  27. Hoffman, K.P. & Stone, J. Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties. Brain Res. 32, 460–466 (1971).

    Article  CAS  Google Scholar 

  28. 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 

  29. Shapley, R., Hawken, M. & Ringach, D.L. Dynamic's of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron 38, 689–699 (2003).

    Article  CAS  Google Scholar 

  30. Sceniak, M.P., Ringach, D.L., Hawken, M.J. & Shapley, R. Contrast's effect on spatial summation by macaque V1 neurons. Nat. Neurosci. 2, 733–739 (1999).

    Article  CAS  Google Scholar 

  31. Cavanaugh, J.R., Bair, W. & Movshon, J.A. Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. J. Neurophysiol. 88, 2530–2546 (2002).

    Article  Google Scholar 

  32. Polat, U., Mizobe, K., Pettet, M.W., Kasamatsu, T. & Norcia, A.M. Collinear stimuli regulate visual responses depending on cell's contrast threshold. Nature 391, 580–584 (1998).

    Article  CAS  Google Scholar 

  33. Kohn, A. & Smith, M.A. Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J. Neurosci. 25, 3661–3673 (2005).

    Article  CAS  Google Scholar 

  34. Finn, I.M., Priebe, N.J. & Ferster, D. The emergence of contrast-invariant orientation tuning in simple cells of cat visual cortex. Neuron 54, 137–152 (2007).

    Article  CAS  Google Scholar 

  35. Chen, Y., Geisler, W.S. & Seidemann, E. Optimal decoding of correlated neural population responses in the primate visual cortex. Nat. Neurosci. 9, 1412–1420 (2006).

    Article  CAS  Google Scholar 

  36. Bernander, O., Douglas, R.J., Martin, K.A. & Koch, C. Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc. Natl. Acad. Sci. USA 88, 11569–11573 (1991).

    Article  CAS  Google Scholar 

  37. Destexhe, A. & Pare, D. Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J. Neurophysiol. 81, 1531–1547 (1999).

    Article  CAS  Google Scholar 

  38. Weliky, M., Kandler, K., Fitzpatrick, D. & Katz, L.C. Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns. Neuron 15, 541–552 (1995).

    Article  CAS  Google Scholar 

  39. Douglas, R.J. & Martin, K.A. Recurrent neuronal circuits in the neocortex. Curr. Biol. 17, R496–R500 (2007).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to B. Malone, A. Benucci and S. Katzner for help with data collection and valuable discussions. This work was supported by grants from the US National Institutes of Health (EY-17396 to M.C., EY-12816 and EY-18322 to D.L.R.) and DARPA (FA8650-06-C-7633 to D.L.R.), an Oppenheimer/Stein Endowment Award (D.L.R.), a Scholar Award from the McKnight Endowment Fund for Neuroscience (M.C.) and a Leopoldina fellowship (BMBF-LPD9901/8-165 to L.B.). M.C. holds the GlaxoSmithKline/Fight for Sight Chair in Visual Neuroscience.

Author information

Authors and Affiliations

  1. Biomedical Engineering Department, University of California Los Angeles, 405 Hilgard Avenue, Los Angeles, 90095, California, USA

    Ian Nauhaus & Dario L Ringach

  2. Smith-Kettlewell Eye Research Institute, 2318 Fillmore Street, San Francisco, 94115, California, USA

    Laura Busse & Matteo Carandini

  3. UCL Institute of Ophthalmology, University College London, 11-43 Bath Street, London, EC1V 9EL, UK

    Matteo Carandini

  4. Departments of Neurobiology University of California Los Angeles, 405 Hilgard Avenue, Los Angeles, 90095, California, USA

    Dario L Ringach

  5. Psychology, University of California Los Angeles, 405 Hilgard Avenue, Los Angeles, 90095, California, USA

    Dario L Ringach

Authors
  1. Ian Nauhaus
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Busse
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matteo Carandini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dario L Ringach
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed in the execution of the experiments, the analysis of the data and the writing of the manuscript.

Corresponding author

Correspondence to Ian Nauhaus.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1 and 2 (PDF 865 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nauhaus, I., Busse, L., Carandini, M. et al. Stimulus contrast modulates functional connectivity in visual cortex. Nat Neurosci 12, 70–76 (2009). https://doi.org/10.1038/nn.2232

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2232

This article is cited by

Search

Advanced 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