Mental images from long-term memory differ from perception: evidence for distinct spatial formats and distinct mechanisms of spatial attention orientation

How is spatial attention deployed in mental images? Mental imagery is often assumed to share mechanisms with visual perception and visual working memory. Top-down, endogenous spatial attention in both visual perception and working memory modulates behaviour and parieto-occipital alpha-band activity. However, working memory captures only a subset of mental imagery, which can also draw upon long-term memory. Here, we ask whether and how spatial attention operates in mental images derived from general knowledge in long-term memory, and whether it recruits the same neural mechanisms as visual perception. We recorded EEG in 28 healthy volunteers (13 males, 15 females) as they performed two discrimination tasks with spatial cues (70% valid): one involving the mental visualization of a long-term memory map (a map of France) and the other using visual stimuli. We show that spatial attention shortens response times in both tasks, but through distinct mechanisms. Behavioural attentional benefits were uncorrelated across tasks, and spatial attention in mental imagery engaged distinct neural mechanisms, with frontal rather than posterior alpha activity modulation. We further reveal fundamental differences in the spatial structures of mental imagery and visual perception. Altogether, our results show that mental images drawn from long-term semantic memory are spatially organized and are amenable to spatial attention deployment, but the underlying neural mechanisms differ from those of visual perception. Our results thus point to marked differences between mental imagery from long-term memory and visual perception. Significance statement Do we orient attention in the mind’s eye as we do in visual perception? For mental images held in working memory, short-lived and percept-like, this seems to be the case. Yet many forms of imagery, such as imagining a map, draw on long-term memory. Our study reveals that spatial attention can also operate within mental images based on long-term memory, but through neural mechanisms distinct from visual perception. Additionally, we show that while these images possess a spatial organization, it does not replicate the spatial format of visual percepts. These findings challenge the assumption that mental imagery simply reuses perceptual processes.