A cortical hierarchical mechanism for subjective visual experience during working memory

Abstract

Working memory (WM) provides a mental sketchpad for simulating sensory experiences associated with mnemonic content. A critical unresolved question is how the brain generates the subjective sensory experience of these internal simulations. Here, we studied individuals with aphantasia, who report a subjective inability to generate visual imagery despite normal WM performance, providing a unique dissociation between objective WM performance and conscious subjective experience. During functional MRI, typical imagers and aphantasic individuals generated and maintained WM content from distinct sources (perception, imagery, or illusion) at a specific spatial location. Time-resolved multivariate analyses revealed a cortical hierarchical mechanism underlying the emergence of subjective visual experience in WM. Rather than dysfunctions in a single brain region, we identified a breakdown in feedback along a cortical pathway from the intraparietal sulcus (IPS) through area V3AB to the early visual cortex (EVC) in aphantasia. The IPS showed impaired imagery generation signals and reduced functional connectivity with EVC, whereas the EVC exhibited a general deficit in feedback independent of voluntary control. These impairments together led to weakened and unstable delay-period representations and precluded the transition from visual to mnemonic codes along the hierarchy. Notably, this network mechanism was specific to imagery at contralateral spatial locations, as ipsilateral IPS maintained compensatory, non-visual representations to support successful task performance without accompanying subjective experience. These results collectively demonstrate that the cortical hierarchy from IPS to EVC is critical for conscious mental visualization of memory content during WM maintenance.