Top-down modulation in human visual cortex predicts the stability of a perceptual illusion

Abstract

Conscious perception sometimes fluctuates strongly, even when the sensory input is constant. For example, in motion-induced blindness (MIB), a salient visual target surrounded by a moving pattern suddenly disappears from perception, only to reappear after some variable time. Whereas such changes of perception result from fluctuations of neural activity, mounting evidence suggests that the perceptual changes, in turn, may also cause modulations of activity in several brain areas, including visual cortex. In this study, we asked whether these latter modulations might affect the subsequent dynamics of perception. We used magnetoencephalography (MEG) to measure modulations in cortical population activity during MIB. We observed a transient, retinotopically widespread modulation of beta (12-30 Hz)-frequency power over visual cortex that was closely linked to the time of subjects' behavioral report of the target disappearance. This beta modulation was a top-down signal, decoupled from both the physical stimulus properties and the motor response but contingent on the behavioral relevance of the perceptual change. Critically, the modulation amplitude predicted the duration of the subsequent target disappearance. We propose that the transformation of the perceptual change into a report triggers a top-down mechanism that stabilizes the newly selected perceptual interpretation.

Keywords: beta oscillations; bistable perception; brain dynamics; brain state; perceptual decision-making.

Fig. 1.

Motion-induced blindness (MIB) stimulus, perceptual dynamics, and cortical stimulus response. A: schematic of the MIB illusion. Bottom, stimulus configuration. The small but salient target (yellow disc) was surrounded by a large moving mask (rotating blue grid). The target was presented in different visual field quadrants for different subjects, at an eccentricity of 3°. Top, alternating perception of the target. B: group average frequency distributions of target invisible and target visible durations during magnetoencephalography (MEG; n = 11 subjects). Shaded areas indicate SE. C: cortical response to the MIB stimulus during Stimulus-on-off condition. Scalp maps show topography of 8- to 35-Hz and 60- to 90-Hz modulations (0.25–0.75 s after stimulus onset; see dashed outlines on time-frequency representations). Transparency level indicates clusters of significant modulation (P < 0.05, 2-sided permutation test across subjects, cluster-corrected; n = 10 subjects). Highlighted symbols indicate MEG sensors showing the biggest stimulus response. These sensors are used for the subsequent analyses of overall power modulations (triangles and squares, sensors used for lateralization analyses; Fig. 3). M(f,t), power modulation.

Fig. 2.

Switch-related power modulations over visual cortex. MEG power modulations are shown as time-frequency representations, averaged across trials and subjects. Transparency level highlights clusters of significant modulation (P < 0.05, 2-sided permutation test, cluster-corrected). In A–J, graphs at top and middle correspond to high- and low-frequency ranges, respectively; colored bars at bottom correspond to time course of stimulus components and subjects' reports. Fading indicates variable timing of (instantaneous) stimulus changes with respect to the trigger. Different panels correspond to different experimental conditions and/or different trigger events. Inset scalp maps represent the sensor group used for this analysis. A: MIB, aligned to report. Black bar represents transient time window used for subsequent analyses. B: Replay-active condition, aligned to report. C: Replay-active condition, aligned to stimulus change. Dotted vertical line indicates median reaction time. D: Replay-passive condition, aligned to stimulus change. E: Replay-no-mask condition, aligned to report. F–J: same as A–E, but for target reappearance. Dotted rectangle in D and I shows time-frequency window for Table 1.

Fig. 3.

Widespread beta-power transient over visual cortex encodes report. In A and B, graphs show spectra of mean low-frequency (<35 Hz) power modulation during transient time window (−0.3 to 0.3 s; see Fig. 2A) around report. Colored bars indicate clusters of significant modulation (P < 0.05, 2-sided permutation test, cluster-corrected). A: MIB, Replay-active, and difference (MIB − Replay-active). Inset scalp map represents the sensor group used for this analysis. B: solid line indicates the reappearance − disappearance difference for overall power modulation (i.e., difference between blue and red line in A). Dashed line indicates lateralization contralateral vs. ipsilateral with respect to target hemifield. Triangles and squares in scalp map represent the sensors used for lateralization analyses. Green solid bar represents clusters of significant overall modulation; black bar represents clusters of significant difference between overall modulation and lateralization (P < 0.05, 2-sided permutation test, cluster-corrected). There is no significant frequency cluster for the lateralization. Shaded colored areas indicate SE (n = 11 subjects); shaded gray areas indicate the range of beta-band modulation during MIB (12–30 Hz). C: topographical maps of transient 12- to 30-Hz modulations and disappearance − reappearance differences.

Fig. 4.

Beta power over motor cortex does not encode report. A and B: same as Fig. 3, A and B, but for sensors overlying motor cortex during MIB and Replay-active. A: frequency spectra of MEG power modulation. B: reappearance − disappearance difference for overall power modulation and lateralization contralateral vs. ipsilateral (contra − ipsi) with respect to hand used for report.

Fig. 5.

Beta-power transient over visual cortex is unrelated to motor act. A: opposite mappings of perceptual event to motor act on days 1 and 2. See main text for details. B and C: same as Fig. 3, A and C, but separately for both mappings (i.e., recording days).

Fig. 6.

Beta-power transient predicts stability of MIB illusion. Pearson correlation between beta-power suppression during disappearance report and the duration of the “preceding percept” (i.e., target visible, left) or “succeeding percept” (i.e., target invisible, right). Single-trial percept durations were normalized by each subject's median percept duration (see main text for details). A: MIB. B: Replay-active. Error bars indicate SE (n = 11 subjects).

Fig. 7.

Beta-band MEG power modulation during MIB is not due to microsaccades. A: modulations of microsaccade rate for MIB target disappearance and reappearance. Gray shaded areas represent the intervals used for computing the difference between the number of microsaccades before and around report (rate change). Error bars indicate SE across subjects. B. time-frequency representation of the correlation between microsaccade rate change and MEG power modulation around MIB disappearance and reappearance reports. Transparency level highlights clusters of significant modulation (P < 0.05, 2-sided permutation test, cluster-corrected). Inset scalp map represents the sensor group used for this analysis. C: time-frequency representation of MEG power modulation, selectively averaged across trials without microsaccades between −0.35 and 0.25 s relative to report (dotted outline). Transparency level highlights clusters of significant modulation (P < 0.05, 2-sided permutation test, cluster-corrected). D: frequency spectra of power modulation for disappearance and reappearance in the transient time window for trials without microsaccades in this time window. Red solid bar indicates clusters of significant modulation (P < 0.05, 2-sided permutation test, cluster-corrected).

Fig. 8.

Conceptual model of beta-power transient. A: schematic of the hypothetical process driving the report-related beta-band modulation in visual cortex. During MIB, Replay-active, and Replay-passive, the cortical representation of the target is suppressed, leading to the target's disappearance. The suppression occurs either spontaneously (i.e., due to intrinsic cortical processing in MIB) or in response to the physical target offset (Replay). If the perceptual disappearance is task-relevant (MIB and Replay-active, but not Replay-passive), a central decision process transforms it into a behavioral report. This transformation induces the top-down modulation in visual cortex. The top-down modulation, in turn, alters the state of visual cortex and, hence, the target representation. B: schematic of dynamical algorithm for cortical state change and perceptual stabilization. In both MIB (top) and Replay-active (bottom), the percept (green “ball”) is in the “target visible” valley. Adaption gradually flattens this valley before target disappearance (sequence: t₋₂, t₋₁, t₀). The ball then hops into the “target invisible” valley (perceptual switch, t₁). Behavioral report of this perceptual event induces a state change that deepens the target invisible valley (t₂; red arrows). This, in turn, stabilizes perception during MIB (t₃, top right): When the state change is strong, the percept variable is less likely to move back to the visible valley some time after the switch (t₃). By contrast, during Replay (t₃, bottom right), the physical target reappearance alters the energy landscape (i.e., eliminates the target invisible valley) and thereby prevents the state change at t₂ from affecting the percept duration.