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Synchrony and covariation of firing rates in the primary visual cortex during contour grouping

Abstract

The visual system imposes structure onto incoming information, by grouping image elements of a single object together, and by segregating them from elements that belong to other objects and the background. One influential theory holds that the code for grouping and segmentation is carried by the synchrony of neuronal discharges on a millisecond time scale. We tested this theory by recording neuronal activity in the primary visual cortex (area V1) of monkeys engaged in a contour-grouping task. We found that synchrony was unrelated to contour grouping. The firing rates of V1 neurons are also correlated across trials. We demonstrate that this rate covariation is mainly determined by fluctuations in visual attention. Moreover, we show that rate covariation depends on perceptual grouping, as it is strongest between neurons that respond to features of the same object.

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Figure 1: Neuronal synchrony in area V1 during contour grouping.
Figure 2: Population analysis of synchrony.
Figure 3: Effects of attention.
Figure 4: Covariation of firing rates.
Figure 5: Dependence of synchrony and rate covariation on stimulus configuration.
Figure 6: Influence of task difficulty on the interactions between neurons in area V1.
Figure 7: Pitting task difficulty against binding.
Figure 8: Factors that determine synchrony and rate covariation.

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References

  1. von der Malsburg, C. The what and why of binding: the modeler's perspective. Neuron 24, 95–104 (1999).

    Article  CAS  Google Scholar 

  2. Roelfsema, P.R. & Singer, W. Detecting connectedness. Cereb. Cortex 8, 385–396 (1998).

    Article  CAS  Google Scholar 

  3. Gray, C.M., König, 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 

  4. Singer, W. & Gray, C.M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995).

    Article  CAS  Google Scholar 

  5. Castelo-Branco, M., Goebel, R., Neuenschwander, S. & Singer, W. Neural synchrony correlates with surface segregation rules. Nature 405, 685–689 (2000).

    Article  CAS  Google Scholar 

  6. Brosch, M., Bauer, R. & Eckhorn, R. Stimulus-dependent modulation of correlated high-frequency oscillations in cat visual cortex. Cereb. Cortex 7, 70–76 (1997).

    Article  CAS  Google Scholar 

  7. Gail, A., Brinksmeyer, H.J. & Eckhorn, R. Contour decouples gamma activity across texture representation in monkey striate cortex. Cereb. Cortex 10, 840–850 (2000).

    Article  CAS  Google Scholar 

  8. Kreiter, A.K. & Singer, W. Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J. Neurosci. 16, 2381–2396 (1996).

    Article  CAS  Google Scholar 

  9. Lamme, V.A.F. & Spekreijse, H. Neuronal synchrony does not represent texture segregation. Nature 396, 362–366 (1998).

    Article  CAS  Google Scholar 

  10. Shadlen, M.N. & Movshon, J.A. Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24, 67–77 (1999).

    Article  CAS  Google Scholar 

  11. Thiele, A. & Stoner, G.R. Neuronal synchrony does not correlate with motion coherence in cortical area MT. Nature 421, 366–370 (2003).

    Article  CAS  Google Scholar 

  12. van Kan, P.L.E., Scobey, R.P. & Gabor, A.J. Response covariance in cat visual cortex. Exp.Brain Res. 60, 559–563 (1985).

    Article  CAS  Google Scholar 

  13. Gawne, T.J., Kjaer, T.W., Hertz, J.A. & Richmond, B.J. Adjacent visual complex cells share about 20% of their stimulus-related information. Cereb. Cortex 6, 482–489 (1996).

    Article  CAS  Google Scholar 

  14. Leopold, D.A., Murayama, Y. & Logothetis, N.K. Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb. Cortex 13, 422–433 (2003).

    Article  Google Scholar 

  15. Shadlen, M.N., Britten, K.H., Newsome, W.T. & Movshon, J.A. A computational analysis of the relationship between neuronal and behavioral responses to visual motion. J. Neurosci. 16, 1486–1510 (1996).

    Article  CAS  Google Scholar 

  16. Bair, W., Zohary, E. & Newsome, W.T. Correlated firing in macaque visual area MT: time scales and relationship to behavior. J. Neurosci. 21, 1676–1697 (2001).

    Article  CAS  Google Scholar 

  17. Lee, D., Port, N.L., Kruse, W. & Georgopoulos, A.P. Variability and correlated noise in the discharge of neurons in motor and parietal areas of the primate cortex. J. Neurosci. 18, 1161–1170 (1998).

    Article  CAS  Google Scholar 

  18. Scholte, H.S., Spekreijse, H. & Roelfsema, P.R. The spatial profile of visual attention in mental curve tracing. Vision Res. 41, 2569–2580 (2001).

    Article  CAS  Google Scholar 

  19. Houtkamp, R., Spekreijse, H. & Roelfsema, P.R. The cause of delays in contour integration. Percept. Psychophys. 65, 1136–1144 (2003).

    Article  CAS  Google Scholar 

  20. Roelfsema, P.R., Lamme, V.A.F. & Spekreijse, H. Object-based attention in the primary visual cortex of the macaque monkey. Nature 395, 376–381 (1998).

    Article  CAS  Google Scholar 

  21. Nelson, J.I., Salin, P.A., Munk, M.H.J., Arzi, M. & Bullier, J. Spatial and temporal coherence in cortico-cortical connections: a cross-correlation study in areas 17 and 18 in the cat. Vis. Neurosci. 9, 21–37 (1992).

    Article  CAS  Google Scholar 

  22. Nowak, L.G., Munk, M.H.J., Nelson, J.I., James, A.C. & Bullier, J. Structural basis of cortical synchronization. I. Three types of interhemispheric coupling. J. Neurophysiol. 74, 2379–2400 (1995).

    Article  CAS  Google Scholar 

  23. Frien, A. & Eckhorn, R. Functional coupling shows stronger stimulus dependency for fast oscillations than for low-frequency components in striate cortex of awake monkey. Eur. J. Neurosci. 12, 1466–1478 (2000).

    Article  CAS  Google Scholar 

  24. Maldonado, P.E., Friedman-Hill, S. & Gray, C.M. Dynamics of striate cortical activity in the alert macaque: II. Fast time scale synchronization. Cereb. Cortex 10, 1117–1131 (2000).

    Article  CAS  Google Scholar 

  25. Steinmetz, P.M. et al. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 404, 187–190 (2000).

    Article  CAS  Google Scholar 

  26. Fries, P., Reynolds, J.H., Rorie, A.E. & Desimone, R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560–1563 (2001).

    Article  CAS  Google Scholar 

  27. Tiitinen, H. et al. Selective attention enhances the auditory 40-Hz transient response in humans. Nature 364, 59–60 (1993).

    Article  CAS  Google Scholar 

  28. Frien, A., Eckhorn, R., Bauer, R., Woelbern, T. & Kehr, H. Stimulus-specific fast oscillations at zero phase between visual areas V1 and V2 of awake monkey. Neuroreport 5, 2273–2277 (1994).

    Article  CAS  Google Scholar 

  29. Friedman-Hill, S., Maldonado, P.E. & Gray, C.M. Dynamics of striate cortical activity in the alert macaque: I. incidence and stimulus dependence of gamma-band neuronal oscillations. Cereb. Cortex 10, 1105–1116 (2000).

    Article  CAS  Google Scholar 

  30. Supèr, H., van der Togt, C., Spekreijse, H. & Lamme, V.A.F. Internal state of monkey primary visual cortex (V1) predicts figure–ground perception. J. Neurosci. 23, 3407–3414 (2003).

    Article  Google Scholar 

  31. Gur, M. & Snodderly, D.M. Studying striate cortex neurons in behaving monkeys: benefits of image stabilization. Vision Res. 27, 2081–2087 (1987).

    Article  CAS  Google Scholar 

  32. König, P. A method for the quantification of synchrony and oscillatory properties of neuronal activity J. Neurosci. Meth. 54, 31–37 (1994).

    Article  Google Scholar 

  33. Roelfsema, P.R., Engel, A.K., König, P. & Singer, W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385, 157–161 (1997).

    Article  CAS  Google Scholar 

  34. Roelfsema, P.R. & Spekreijse, H. The representation of erroneously perceived stimuli in the primary visual cortex. Neuron 31, 853–863 (2001).

    Article  CAS  Google Scholar 

  35. Roelfsema, P.R., Lamme, V.A.F. & Spekreijse, H. The implementation of visual routines. Vision Res. 40, 1385–1411 (2000).

    Article  CAS  Google Scholar 

  36. Treisman, A.M. & Gelade, G. A feature-integration theory of attention. Cogn. Psychol. 12, 97–136 (1980).

    Article  CAS  Google Scholar 

  37. Duncan, J. Selective attention and the organization of visual information. J. Exp. Psychol. Gen. 113, 501–517 (1984).

    Article  CAS  Google Scholar 

  38. Sigman, M., Cecchi, G.A., Gilbert, C.D. & Magnasco, M.O. On a common circle: natural scenes and Gestalt rules. Proc. Natl. Acad. Sci. USA 98, 1935–1940 (2001).

    Article  CAS  Google Scholar 

  39. Kellman, P.J. & Shipley, T.F. A theory of visual interpolation in object perception. Cogn. Psychol. 23, 141–221 (1991).

    Article  CAS  Google Scholar 

  40. Sporns, O., Gally, J.A., Reeke, G.N., Jr. & Edelman, G.M. Reentrant signaling among simulated neuronal groups leads to coherency in their oscillatory activity. Proc. Natl. Acad. Sci. USA 86, 7265–7269 (1989).

    Article  CAS  Google Scholar 

  41. Bosking, W.H., Zhang, Y., Schofield, B. & Fitzpatrick, D. Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J. Neurosci. 15, 2112–2127 (1997).

    Article  Google Scholar 

  42. Schmidt, K.E., Goebel, R., Löwel, S. & Singer, W. The perceptual grouping criterion of colinearity is reflected by anisotropies of connections in the primary visual cortex. Eur. J. Neurosci. 9, 1083–1089 (1997).

    Article  CAS  Google Scholar 

  43. 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 

  44. Worden, M.S., Foxe, J.J., Wang, N. & Simpson, G.V. Anticipatory biasing of visuospatial attention indexed by retinotopically specific α-band electroencephalography increases over occipital cortex. J. Neurosci. 20, RC63:1–6 (2000).

    Article  Google Scholar 

  45. Posner, M.I. & Petersen, S.E. The attentional system of the human brain. Annu. Rev. Neurosci. 13, 25–42 (1990).

    Article  CAS  Google Scholar 

  46. Büchel, C. & Friston, K. Assessing interactions among neuronal systems using functional imaging. Neural Net. 13, 871–882 (2000).

    Article  Google Scholar 

  47. McIntosh, A.R., Rajah, M.N. & Lobaugh, N.J. Interactions of prefrontal cortex in relation to awareness in sensory learning. Science 284, 1531–1533 (1999).

    Article  CAS  Google Scholar 

  48. Lamme, V.A.F. & Roelfsema, P.R. The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci. 23, 571–579 (2000).

    Article  CAS  Google Scholar 

  49. Oram, M.W., Földiák, P., Perrett, D.I. & Sengpiel, F. The 'ideal homunculus': decoding neural population signals. Trends Neurosci. 21, 259–265 (1998).

    Article  CAS  Google Scholar 

  50. Verghese, P. & Stone, L.S. Perceived visual speed constrained by image segmentation. Nature 381, 161–163 (1996).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J.C. de Feiter and K. Brandsma for technical assistance. We thank P. König and C. van der Togt for comments on an earlier version of the manuscript. This work was supported by a grant from the McDonnell Pew Program in Cognitive Neuroscience, and a grant of the Human Frontier Science Program.

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Correspondence to Pieter R Roelfsema.

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Supplementary information

Supplementary Fig. 1

Visual responsiveness at A-sites and N-sites is similar. (a,b) Population responses at A-sites and N-sites have a similar time course. Responses of neurons at A-sites evoked by the target curve (T) are enhanced relative to responses evoked by the distractor curve (D), but neurons at N-sites do not discriminate between the two curves. (c,d) Comparison of the reliability of visual responses at A- and N-sites with an ROC-analysis. The distribution of spontaneous activity across single trials in a 50 ms window (from 300-250 ms before stimulus appearance) was compared to the single-trial distributions of visually evoked activity in successive 50 ms bins. The area under the ROC-curve provides a measure for the reliability of the visual response. It equals 1.0 if 50 ms of activity in a single trial is sufficient to be confident that there is a contour in the RF, and 0.5 if the distribution of visually evoked activity is similar to the distribution of spontaneous activity. The ROC-area was averaged across all A-sites (c) and N-sites (d). It reaches almost 1.0 during the transient response and plateaus at a somewhat lower value during the sustained response phase. The ROC-area at N-sites is similar to the ROC-area associated with responses evoked by the distractor curve at A-sites (P>0.2, U-test). (PDF 13 kb)

Supplementary Fig. 2

Errors in perceptual grouping do not influence synchrony. (a) 43 cases where the RFs fell on contours of the same curve and on opposite sides of the critical zone (switching partners). For these cases, at least 20 erroneous and 20 correct trials were obtained with the same stimulus configuration. On correct trials, the RF-contours were grouped in the monkey's perception and on error trials they were not. Synchrony on error trials does not differ significantly from synchrony on correct trials (paired t-test, t42=−0.5, P>0.2). Cases without significant synchrony in both conditions are superimposed on the origin. (b) 25 cases where RFs fell on contours of different curves. On correct trials, the monkey assigned these contours to different curves, but on error trials they were mistakenly grouped together. Again, synchrony did not differ between correct and error trials (paired t-test, t24=−0.3, P>0.2). (PDF 23 kb)

Supplementary Fig. 3

Recording technique. (a) The signal coming from the chronically implanted electrodes is amplified and filtered between 750 and 5000 Hz (Filt1). Single unit activity (SUA) and multi-unit activity (MUAS) are obtained by detecting times at which Filt1 reaches a threshold with a Schmidt trigger. To obtain MUAE, Filt1 is full-wave rectified (negative potentials become positive), low-pass filtered at 500 Hz (Filt2), and sampled at a rate of 1000 or 1100 Hz. (b) In this case SUA can be recorded by suitable positioning of the trigger level (red dashed line). The shapes of the action potentials that are detected in this way are similar (not shown). If the trigger level is lowered, MUAS is recorded (blue dashed line). The inset shows all these signals at higher temporal resolution. The shaded region that is superimposed on Filt1 replicates MUAE, to illustrate that it follows the signal's envelope. MUAE is large whenever neurons in the vicinity of the electrode fire action potentials. (PDF 941 kb)

Supplementary Methods (PDF 1013 kb)

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Roelfsema, P., Lamme, V. & Spekreijse, H. Synchrony and covariation of firing rates in the primary visual cortex during contour grouping. Nat Neurosci 7, 982–991 (2004). https://doi.org/10.1038/nn1304

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