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Clinical Trial
.1999 Jul 1;19(13):5435-48.
doi: 10.1523/JNEUROSCI.19-13-05435.1999.

Increased synchronization of neuromagnetic responses during conscious perception

Affiliations
Clinical Trial

Increased synchronization of neuromagnetic responses during conscious perception

R Srinivasan et al. J Neurosci..

Abstract

In binocular rivalry, the observer views two incongruent images, one through each eye, but is conscious of only one image at a time. The image that is perceptually dominant alternates every few seconds. We used this phenomenon to investigate neural correlates of conscious perception. We presented a red vertical grating to one eye and a blue horizontal grating to the other eye, with each grating continuously flickering at a distinct frequency (the frequency tag for that stimulus). Steady-state magnetic fields were recorded with a 148 sensor whole-head magnetometer while the subjects reported which grating was perceived. The power of the steady-state magnetic field at the frequency associated with a grating typically increased at multiple sensors when the grating was perceived. Changes in power related to perceptual dominance, presumably reflecting local neural synchronization, reached statistical significance at several sensors, including some positioned over occipital, temporal, and frontal cortices. To identify changes in synchronization between distinct brain areas that were related to perceptual dominance, we analyzed coherence between pairs of widely separated sensors. The results showed that when the stimulus was perceived there was a marked increase in both interhemispheric and intrahemispheric coherence at the stimulus frequency. This study demonstrates a direct correlation between the conscious perception of a visual stimulus and the synchronous activity of large populations of neocortical neurons as reflected by stimulus-evoked steady-state neuromagnetic fields.

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Figures

Fig. 1.
Fig. 1.
Episode durations of perceptual dominance of the red vertical and blue horizontal gratings, averaged over the eight rivalry trials of subject (J.S.).
Fig. 2.
Fig. 2.
Left, Amplitude spectra of a single rivalry trial in subject J.S. at MEG sensors located over the left frontal (A), left parietal-central (B), and right occipital (C) cortex. Note the sharp peak at 7.41 Hz, the flicker frequency of the red grating, and at 8.33 Hz, the flicker frequency of the blue grating. The peaks are confined to one frequency bin, Δf = 0.0032 Hz (aliasing artifacts by the graphing software sometimes create the appearance of additional bins). The SNR, defined as the ratio of the power at the peak to the average power in a 0.06 Hz band (20 bins) surrounding it, is indicated on each plot for the 7.41 Hz peak. Only those peaks satisfying a criterion of SNR >5 were submitted to further analysis.Right, Topographic display of the signal amplitude at the common stimulus flicker frequency offc = 7.41 Hz, averaged across all eight rivalry trials. Although signal power is discussed in the text, the square root of the power, equivalent to the absolute magnitude of the field amplitude, is plotted here to increase the displayed dynamic range. The topographic maps were generated by interpolating the amplitude values at the 148 sensors on a best-fit sphere with a three-dimensional spline. The map is then projected from the sphere onto a plane. The positions on the best-fit sphere of sensors with SNR >5 are indicated byopen circles. A few points are designated based on the 10–20 EEG electrode placement system:F, frontal;C, central;P, parietal;O, occipital; andT, temporal. The channels labeledA–C (filled blue dots) correspond to the amplitude spectra shown on theleft. Contours of constant amplitude (A) are indicated in steps of 0.2 picotesla;dashed lines are forA < 1 picotesla, andsolid lines are forA≥ 1 picotesla.
Fig. 3.
Fig. 3.
Analysis of the temporal offset between subject J.S.’s response functions and steady-state power differences. The power spectrum was calculated with the response function offset from the MEG data by an offset time τ ranging from −2.5 to +2.5 sec in steps of 0.25 sec. All plots show power at the single frequencyfc = 7.41 Hz that was used in all eight rivalry trials and four stimulus-alternation trials.A, Power difference as a function of offset time and channel number for the stimulus-alternation trials. Thecontour lines inmagenta indicate positive power differences (power is greater during episodes reported as dominant by the subject);green lines indicate negative differences in power.Contour lines are shown at 0.05 picotesla2 and are higher in steps of 0.025 picotesla2.B, Topographic display of amplitude corresponding to perceptual dominance (top) and to perceptual nondominance (bottom) for stimulus-alternation trials, at the offset for which the difference was maximal (τ = 0.25 sec). There is essentially no power during nondominance, because no stimulus is presented at that frequency during those intervals.C, Power difference for the rivalry trials, plotted as described inA.D, Topographic display of amplitude for the rivalry trials, plotted as described inB. During rivalry the offset for which the difference was maximal was τ = 1.0 sec. Note that for rivalry trials there is still considerable power during nondominance, even though the stimulus is not perceived.
Fig. 4.
Fig. 4.
Left, Topographic display of amplitude differences (ΔA) atfc = 7.41 Hz between perceptual dominance and nondominance for subject J.S.Contours of constant ΔA are indicated in steps of 0.2 picotesla;dashed lines are for ΔA < 0 picotesla, andsolid lines are for ΔA ≥ 0 picotesla. Thecirclesindicate channels with SNR >5. Thecircles filled ingreen indicate channels that were individually significant after Bonferroni correction (p< 0.05).Top right, Distribution of permutation samples of the summed squared power difference. Permutation samples were obtained by randomizing the pairing between MEG records and the response functions, yielding 8! (= 40320) samples including the observed pairing. The power difference was squared and summed over all channels with SNR >5 (n = 80). Thered bar indicates the observed power difference that has significancep < 0.005, as determined from the permutation distribution.Bottom right, Histogram of permutation samples of the power difference at a single channel. The observed difference is indicated by agreen bar. After Bonferroni correction, this difference was significant atp < 0.05. The channel shown is indicated by ablue dot on the topographic map.
Fig. 5.
Fig. 5.
Topographic display of the average amplitude differences between perceptual dominance and nondominance in seven subjects. The common frequency was 7.41 Hz for all subjects except R.G., for whom it was 8.33 Hz. The omnibus significance of the maps, which was calculated using only channels with SNR >5 (indicated by acircle), wasp < 0.005 for all subjects except G.A. and M.T. For these two subjects the overall SNR was lower. Using the channels with SNR >2, their omnibus significance wasp < 0.05. Individual channels that reached a Bonferroni-corrected significance ofp < 0.05 are indicated in all subjects by afilled green circle.
Fig. 6.
Fig. 6.
Scatter diagrams of coherence versus sensor separation for subject S.P. Sensor-separation distances were calculated on the best-fit sphere to the sensor positions. This sphere has a radius of 12 cm, and the typical separation between neighboring sensors is 3 cm. The stimulus frequency isfc = 7.41 Hz. The frequency resolution for the coherence calculations was Δf = 0.016 Hz. Only sensors with SNR >5 were included.Top left, Scatter plot for the frequencyfc − 10Δf.Top right, Scatter plot for the frequencyfc − Δf.Bottom left, Scatter plot for the frequencyfc + Δf.Bottom right, Scatter plot for the frequencyfc. Note that at all three unstimulated frequencies the coherence exhibits the same steep decrease with sensor separation, becoming negligible at sensor separations of >12 cm. At the stimulus frequency, coherence is generally >0.5 at all separations.
Fig. 7.
Fig. 7.
Scatter diagrams of coherence versus sensor separation corresponding to perceptual dominance and nondominance for subject S.P. The scatter plots are described in Figure 6.Top left, Scatter plot for the frequencyfc − Δf during perceptual dominance.Top right, Scatter plot for the frequencyfc during perceptual dominance.Bottom left, Scatter plot for the frequencyfc − Δf during perceptual nondominance.Bottom right, Scatter plot for the frequencyfc during perceptual nondominance. Note that at the unstimulated frequency the coherence is not modulated by perceptual dominance.
Fig. 8.
Fig. 8.
Scatter diagrams of the coherence difference versus the geometric mean of the magnitude of the power difference between perceptual dominance and nondominance for subjects S.P. and F.G. The coherences shown are between sensors with SNR >5 and separated by at least 12 cm. In each plot, theblue circles correspond to sensor pairs in which perceptual dominance increased the power at both sensors. Thered triangles correspond to sensor pairs in which power decreased at both sensors. Thegreen squares correspond to sensor pairs in which one increased power and one decreased power. Thefilled symbols indicate robust coherence differences.Left, Coherence differences versus the geometric mean of the magnitude of power differences in subject S.P. For each sensor pair, the geometric mean is the square root of the product of the absolute values of the power differences.Right, A plot the same asleft for subject F.G. The figures demonstrate that the size and direction of coherence modulation do not depend on the power modulation.
Fig. 9.
Fig. 9.
Topography of coherence during perceptual dominance and nondominance in subject S.P.Top left, Coherence matrix during perceptual dominance. In this channel-by-channel matrix, the channels are sorted into groups:LA, left anterior;LP, left posterior;RP, right posterior; andRA, right anterior.Top right, Coherence matrix during perceptual nondominance.Bottom left, Coherence difference matrix obtained by subtracting coherence during perceptual nondominance from coherence during perceptual dominance. Note that most of the coherences are higher during dominance. The summed squared coherence differences were significant (p < 0.005) as determined by the use of a randomization test.Bottom right, Topography of robust coherence differences. The topographic map shows the amplitude difference between dominance and nondominance.Filled green circles indicate channels with SNR >5 and a coherence >0.3 with at least one other channel. Robust differences between perceptual dominance and nondominance are indicated bycyan lines for positive differences andblue lines for negative differences. Robust differences in coherence were defined as those in which the difference exceeded twice the SE of the overall coherence.
Fig. 10.
Fig. 10.
Coherence differences in four subjects.Left, Coherence difference matrices, plotted as described in Figure 9. Note that most coherences are higher during dominance. The summed squared coherence differences were significant (p < 0.05) in each subject as determined by the use of a randomization test.Right, Topographic map of robust coherence differences, plotted as described in Figure9.
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