Research into the neural correlates of individual differences in imagery vividness point to an important role of the early visual cortex. However, there is also great fluctuation of vividness within individuals, such that only looking at differences between people necessarily obscures the picture. In this study, we show that variation in moment-to-moment experienced vividness of visual imagery, within human subjects, depends on the activity of a large network of brain areas, including frontal, parietal, and visual areas. Furthermore, using a novel multivariate analysis technique, we show that the neural overlap between imagery and perception in the entire visual system correlates with experienced imagery vividness. This shows that the neural basis of imagery vividness is much more complicated than studies of individual differences seemed to suggest.SIGNIFICANCE STATEMENTVisual imagery is the ability to visualize objects that are not in our direct line of sight: something that is important for memory, spatial reasoning, and many other tasks. It is known that the better people are at visual imagery, the better they can perform these tasks. However, the neural correlates of moment-to-moment variation in visual imagery remain unclear. In this study, we show that the more the neural response during imagery is similar to the neural response during perception, the more vivid or perception-like the imagery experience is.

Research suggests that perception and imagination engage neuronal representations in the same visual areas. However, the underlying mechanisms that differentiate sensory perception from imagination remain unclear. Here, we examine the directed coupling (effective connectivity) between fronto-parietal and visual areas during perception and imagery. We found an increase in bottom-up coupling during perception relative to baseline and an increase in top-down coupling during both perception and imagery, with a much stronger increase during imagery. Modulation of the coupling from frontal to early visual areas was common to both perception and imagery. Furthermore, we show that the experienced vividness during imagery was selectively associated with increases in top-down connectivity to early visual cortex. These results highlight the importance of top-down processing in internally as well as externally driven visual experience.

Visual perception and imagery rely on similar representations in the visual cortex. During perception, visual activity is characterized by distinct processing stages, but the temporal dynamics underlying imagery remain unclear. Here, we investigated the dynamics of visual imagery in human participants using magnetoencephalography. Firstly, we show that, compared to perception, imagery decoding becomes significant later and representations at the start of imagery already overlap with later time points. This suggests that during imagery, the entire visual representation is activated at once or that there are large differences in the timing of imagery between trials. Secondly, we found consistent overlap between imagery and perceptual processing around 160 ms and from 300 ms after stimulus onset. This indicates that the N170 gets reactivated during imagery and that imagery does not rely on early perceptual representations. Together, these results provide important insights for our understanding of the neural mechanisms of visual imagery.

Humans are voracious imaginers, with internal simulations supporting memory, planning and decision-making. Because the neural mechanisms supporting imagery overlap with those supporting perception, a foundational question is how reality and imagination are kept apart. One possibility is that the intention to imagine is used to identify and discount self-generated signals during imagery. Alternatively, because internally generated signals are generally weaker, sensory strength is used to index reality. Traditional psychology experiments struggle to investigate this issue as subjects can rapidly learn that real stimuli are in play. Here, we combined one-trial-per-participant psychophysics with computational modelling and neuroimaging to show that imagined and perceived signals are in fact intermixed, with judgments of reality being determined by whether this intermixed signal is strong enough to cross a reality threshold. A consequence of this account is that when virtual or imagined signals are strong enough, they become subjectively indistinguishable from reality.