Reconstructing Spatio-Temporal Trajectories of Visual Object Memories in the Human Brain

Abstract

How the human brain reconstructs, step-by-step, the core elements of past experiences is still unclear. Here, we map the spatiotemporal trajectories along which visual object memories are reconstructed during associative recall. Specifically, we inquire whether retrieval reinstates feature representations in a copy-like but reversed direction with respect to the initial perceptual experience, or alternatively, this reconstruction involves format transformations and regions beyond initial perception. Participants from two cohorts studied new associations between verbs and randomly paired object images, and subsequently recalled the objects when presented with the corresponding verb cue. We first analyze multivariate fMRI patterns to map where in the brain high- and low-level object features can be decoded during perception and retrieval, showing that retrieval is dominated by conceptual features, represented in comparatively late visual and parietal areas. A separately acquired EEG dataset is then used to track the temporal evolution of the reactivated patterns using similarity-based EEG-fMRI fusion. This fusion suggests that memory reconstruction proceeds from anterior frontotemporal to posterior occipital and parietal regions, in line with a conceptual-to-perceptual gradient but only partly following the same trajectories as during perception. Specifically, a linear regression statistically confirms that the sequential activation of ventral visual stream regions is reversed between image perception and retrieval. The fusion analysis also suggests an information relay to frontoparietal areas late during retrieval. Together, the results shed light onto the temporal dynamics of memory recall and the transformations that the information undergoes between the initial experience and its later reconstruction from memory.