Local category-specific gamma band responses in the visual cortex do not reflect conscious perception

Abstract

Which neural processes underlie our conscious experience? One theoretical view argues that the neural correlates of consciousness (NCC) reside in local activity in sensory cortices. Accordingly, local category-specific gamma band responses in visual cortex correlate with conscious perception. However, as most studies manipulated conscious perception by altering the amount of sensory evidence, it is possible that they reflect prerequisites or consequences of consciousness rather than the actual NCC. Here we directly address this issue by developing a new experimental paradigm in which conscious perception is modulated either by sensory evidence or by previous exposure of the images while recording intracranial EEG from the higher-order visual cortex of human epilepsy patients. A clear prediction is that neural processes directly reflecting conscious perception should be present regardless of how it comes about. In contrast, we observed that although subjective reports were modulated both by sensory evidence and by previous exposure, gamma band responses solely reflected sensory evidence. This result contradicts the proposal that local gamma band responses in the higher-order visual cortex reflect conscious perception.

Figure 1.

Experimental paradigm and behavioral results. A, Each block consisted of two phases. In the first phase, half of the images are exposed. In the second phase, pictures are degraded and shown briefly. Degraded pictures from phase 1 are presented together with new pictures (manipulation of previous exposure). Pictures are also shown at two different degradation levels (manipulation of sensory evidence). B, Proportion of “seen” person trials in the four experimental conditions. Error bars indicate SEM.

Figure 2.

Location, spectral profile, and time–frequency representation of an example electrode with person-specific responses in the human visual cortex. An example electrode (see Table 1, electrode 3, for the MNI coordinates) exhibiting person-specific responses overlaid on a coronal view of patient's MRI. Person-specific electrodes were determined by contrasting conditions that included a person in the image with conditions that only included a natural background. Selective responses were observed around the body-selective areas of the human visual cortex. As evident from the power spectra and time–frequency plots, the effect is visible in a broad range of gamma frequencies starting at ∼50 Hz.

Figure 3.

Time course of high-gamma band responses in human visual cortex. A, Trials where subjects reported to have consciously perceived the persons showed higher GBR. B, In the same electrodes, a reliable modulation by sensory evidence is observed, i.e., trials where sensory evidence is stronger also show enhanced GBR. C, However, previous exposure has no effect on GBR despite that subjective reports about conscious perception are increased to the same extent by sensory evidence and previous exposure. Numbers refer to the electrode numbers in Table 1, which provides MNI coordinates and response properties. Error bars indicate SEM.