Spatiotemporal dynamics of self-generated imagery reveal a reverse cortical hierarchy from cue-induced imagery

Abstract

Visual imagery, the ability to generate visual experience in the absence of direct external stimulation, allows for the construction of rich internal experience in our mental world. Most imagery studies to date have focused on cue-induced imagery, namely the to-be-imagined contents were triggered by external cues. It has remained unclear how internal experience derives volitionally in the absence of any external cues, and whether this kind of self-generated imagery relies on an analogous cortical network as cue-induced imagery. Here, leveraging a novel self-generated imagery paradigm, we systematically examined the spatiotemporal dynamics of self-generated imagery, by having participants volitionally imagining one of the orientations from a learned pool; and of cue-induced imagery, by having participants imagining line orientations based on associative cues acquired previously. Using electroencephalography (EEG) and functional magnetic resonance imaging (fMRI), in combination with multivariate encoding and decoding approaches, our results revealed largely overlapping neural signatures of cue-induced and self-generated imagery in both EEG and fMRI; yet, these neural signatures displayed substantially differential sensitivities to the two types of imagery: self-generated imagery was supported by an enhanced involvement of anterior cortex in generating and maintaining imagined contents, as evidenced by enhanced neural representations of orientations in sustained potentials in central channels in EEG, and in posterior frontal cortex in fMRI. By contrast, cue-induced imagery was supported by enhanced neural representations of orientations in alpha-band activity in posterior channels in EEG, and in early visual cortex in fMRI. These results jointly support a reverse cortical hierarchy in generating and maintaining imagery contents in self-generated versus externally-cued imagery.