Investigating neural correlates of conscious perception by frequency-tagged neuromagnetic responses - PubMed (original) (raw)

Investigating neural correlates of conscious perception by frequency-tagged neuromagnetic responses

G Tononi et al. Proc Natl Acad Sci U S A. 1998.

Abstract

In binocular rivalry, a subject views two incongruent stimuli through each eye but consciously perceives only one stimulus at a time, with a switch in perceptual dominance every few seconds. To investigate the neural correlates of perceptual dominance in humans, seven subjects were recorded with a 148-channel magnetoencephalography array while experiencing binocular rivalry. A red vertical grating flickering at one frequency was presented to one eye through a red filter and a blue horizontal grating flickering at a different frequency was presented to the other eye through a blue filter. Steady-state neuromagnetic responses at the two frequencies were used as tags for the two stimuli and analyzed with high-resolution power spectra. It was found that a large number of channels showed peaks at both frequencies, arranged in a horseshoe pattern from posterior to anterior regions, whether or not the subject was consciously perceiving the corresponding stimulus. However, the amount of power at the stimulus frequency was modulated in relation to perceptual dominance, being lower in many channels by 50-85% when the subject was not conscious of that stimulus. Such modulation by perceptual dominance, although not global, was distributed to a large subset of regions showing stimulus-related responses, including regions outside visual cortex. The results demonstrate a correlation between the conscious perception of a visual stimulus and the synchronous activity of large populations of neurons as reflected by steady-state neuromagnetic responses.

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Figures

Figure 1

Figure 1

(Upper Left) High-resolution power-frequency spectra for steady-state evoked potentials recorded over an anterior channel (128) and over a posterior channel (103) during rivalry trials (subject O.S.). Note the sharp peak at 7.41 Hz (f1), the flicker frequency of s1, as well as at 8.33 Hz (f2), the flicker frequency of s2. The peak is confined to 1 frequency bin (0.0032 Hz). The SNR, defined as the ratio of the power at the peak and the average power in a 0.06 Hz band (40 bins) surrounding it, is 25.0 (7.41 Hz, anterior channel), 29.7 (8.33 Hz, anterior channel), 39.2 (7.41 Hz, posterior channel), and 48.9 (8.33 Hz, posterior channel). A broad-band peak in the alpha range is visible at the posterior channel. (Upper Right) Schematic topographic representation of the 148 channels in the MEG array. For convenience, a few points designated based on the ten-twenty electrode placement system are superimposed: F, frontal; C, central; P, parietal; O, occipital; and T, temporal. The locations of channels 128 and 103 are indicated by filled blue circles. (Lower) Topographic display of signal power at the stimulus flicker frequency of 7.41 Hz. The topographic maps were generated by interpolating the amplitude values (square root of power) at 148 sensors on a best-fit sphere with a three dimensional spline. The sensor positions on the best-fit sphere are indicated by dots. The map is then projected from the sphere onto a plane. Channels meeting a SNR criterion of at least 2 are indicated by an open circle. (Left) Stimulus-alternation trials. In this and in the subsequent figures, the values represent an average of four trials. (Right) Rivalry trials. In this and the subsequent figures, the values represent an average of eight trials in which the stimulus flicker frequency 7.41 Hz was associated with either the red vertical grating or the blue horizontal grating and presented to either the right or the left eye (see Materials and Methods). Note the typical horseshoe distribution of the peak in power at 7.41 Hz, which is similar under stimulus-alternation and rivalry conditions (subject O.S.). Solid contour lines begin at 1 picotesla in steps of 0.1 picoteslas. Dashed contour lines range from 0 to 0.9 picoteslas.

Figure 2

Figure 2

Power difference values between perceptual dominance and nondominance for all channels at different offsets (τ) of the response function. (Left) Stimulus-alternation trials. The contour lines in magenta indicate a positive difference in power, while green lines indicate a negative difference in power. The magnitude of the power difference is indicated by the number of contour lines. Contour lines begin at 0.05 picotesla2 in steps of 0.025 picotesla2. (Right) Rivalry trails (subject O.S.). Note that for most channels the maximum power difference occurs at τ = 0.25 sec for stimulus-alternation trials, and at τ = 0.75 sec for rivalry trials.

Figure 3

Figure 3

Topographic display of power at 7.41 Hz corresponding to perceptual dominance (Top), to perceptual nondominance (Middle), and to the difference in power between dominance and nondominance (Bottom), at the offset for which the difference was maximal. Amplitude values (square root of power) are plotted. (Left) Stimulus-alternation trials. During nondominance, there is no amplitude contribution at the frequency of the absent stimulus. The difference in amplitude is coextensive with the distribution of stimulus-related responses. (Right) Rivalry trials. Note that the distribution of stimulus-related responses during nondominance is similar to that during dominance. Many channels show, however, amplitude values that are lower by 50–85% during nondominance. A positive difference in amplitude between perceptual dominance and nondominance is observed bilaterally at occipital, temporal, and frontal channels (subject O.S.). The omnibus significance of the map was computed as described in Materials and Methods (P < 0.05).

Figure 4

Figure 4

Topographic display of power differences between perceptual dominance and nondominance in four other subjects. Amplitude values (square root of power) are plotted. The frequency tested for each subject was: R.G. (8.33 Hz), S.P. (7.41 Hz), L.G. (7.41 Hz), and M.T. (7.41 Hz). The values are based on eight runs counterbalanced across eyes and color. The omnibus significance of the maps was P < 0.005 for all subjects.

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