Why thinking over & over about something leads to ever more thoughts about it: Future voluntary imagery can be decoded from activity patterns in the brain up to 11 secs before engaging in voluntary imagery

Decoding the contents and strength of imagery before volitional engagement. Roger Koenig-Robert & Joel Pearson. Scientific Reports, volume 9, Article number: 3504 (2019). https://www.nature.com/articles/s41598-019-39813-y

Abstract: Is it possible to predict the freely chosen content of voluntary imagery from prior neural signals? Here we show that the content and strength of future voluntary imagery can be decoded from activity patterns in visual and frontal areas well before participants engage in voluntary imagery. Participants freely chose which of two images to imagine. Using functional magnetic resonance (fMRI) and multi-voxel pattern analysis, we decoded imagery content as far as 11 seconds before the voluntary decision, in visual, frontal and subcortical areas. Decoding in visual areas in addition to perception-imagery generalization suggested that predictive patterns correspond to visual representations. Importantly, activity patterns in the primary visual cortex (V1) from before the decision, predicted future imagery vividness. Our results suggest that the contents and strength of mental imagery are influenced by sensory-like neural representations that emerge spontaneously before volition.

Introduction

A large amount of psychology and, more recently, neuroscience has been dedicated to examining the origins, dynamics and categories of thoughts1,2,3. Sometimes, thoughts feel spontaneous and even surprising; while other times they feel effortful, controlled and goal oriented. When we decide to think about something, how much of that thought is biased by pre-existent neural activity? Mental imagery, a sensory thought, can be triggered voluntarily or involuntarily4. However, how much of the content and strength of our mental images we actually control when we voluntarily generate imagery remains unknown. For example, individuals with post-traumatic stress disorder (PTSD) report a complete lack of control of both the content and strength of their mental imagery5. While evidence suggests that imagery strength varies both between and within individuals in the normal population5,6. Previous research has shown that prefrontal activity can predict future decisions7,8,9,10, and nonconscious sensory activity11, and that mental images can be decoded from early visual cortex12,13. However, it remains unknown whether nonconscious sensory activity influences what we think and how strongly we think it.

To investigate the origins of the content and strength of voluntary imagery, we crafted a thought-based mental imagery decision task, in which individuals could freely decide what to imagine, while we recorded brain activation using functional magnetic resonance imaging (fMRI). We used multi-voxel pattern analysis (MVPA, see Materials and Methods for details) to decode information contained in spatial patterns of brain activation recorded using fMRI14,15,16. Additionally, in an independent control experiment, we estimated the temporal reliability of the reported onset of thoughts, as it has been criticized in previous paradigms17. Using a design exploiting the known effect of imagery priming on subsequent binocular rivalry as a function of time18, we show that participants’ reports of thought onsets were indeed reliable within the temporal resolution of fMRI.

Models of determinants of decision making postulate that executive areas in the prefrontal cortex would trigger selection processes leading to future choices9,10,19. In addition to the executive areas involvement in future visual thoughts, we aimed to test whether predictive information could also be decoded from visual areas, as previous results have shown that visual imagery recruits visual areas12,13. To test this, we used both searchlight and visual (from V1 to V4) regions-of-interest (ROI) decoding. We also sought to determine the representational content of the predictive signals: is predictive information, to some extent, similar to perceptual visual representations? To assess this, we perceptually presented gratings outside of attention to participants in separate runs. Functional brain images from the perceptual blocks were then used to train classifiers, which were subsequently tested on imagery blocks both before and after the decision. This so called perception-imagery generalization cross decoding was thus used to show common informational content between visual perceptual representations and predictive signals. Finally, we tested whether the subjective strength of visual imagery could be decoded from information in visual areas before reported volition. Such an involvement of visual areas in the future strength of visual imagery would provide further evidence that sensory areas also play an important role in the phenomenology of future thoughts.

Using this paradigm, we found that activity patterns were predictive of mental imagery content as far back as 11 seconds before the voluntary decision of what to imagine –in visual, frontal and subcortical areas. Importantly, predictive patterns in the primary visual cortex (V1) and the lateral prefrontal cortex were similar to perceptual representations elicited by unattended images. We show that the subjective strength (vividness) of future mental imagery can be predicted from activation patterns contained in the primary visual cortex (V1) before a decision is made. Our results suggest that the contents and strength of mental imagery are influenced by sensory-like neural representations that emerge spontaneously before volition. These results are important as they point to a role of visual areas in the pre-volitional processes leading to visual thought production, thus shedding light on the mechanisms of intrusive mental imagery in conditions such as PTSD, as well as the origins of normal mental imagery.

Concluding remarks and future directions

Our current study can be seen as the first to capture the possible origins and contents of involuntary thoughts and how they progress into or bias subsequent voluntary imagery. This is compatible with the finding that the most prominent differences between low and high vividness trials are seen for the pre-imagery period in visual areas, especially the primary visual cortex, which can be interpreted as when one of the patterns is more strongly represented it will induce a more vivid subsequent volitional mental image. This is in line with reports showing that imagery vividness depends on the relative overlap of the patterns of activation elicited by visual perception and imagery45. Our results expand that finding by showing that the vividness of future visual thoughts is predicted by information stored in the primary visual cortex.

It is up to future research to reveal whether representations biasing subsequent voluntary imagery are genuinely non-conscious or not. This will not only shed light on age-old questions of volition, but also provide a clear mechanism for pathological intrusive thoughts common across multiple mental disorders.