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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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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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)
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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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DOI: https://doi.org/10.1038/nn1304
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