Eye-movement reinstatement and neural reactivation during mental imagery

Abstract

5Half a century ago, Donald Hebb posited that mental imagery is a constructive process that 6 emulates perception. Specifically, Hebb claimed that visual imagery results from the reactivation 7 of neural activity associated with viewing images. He also argued that neural reactivation and 8 imagery benefit from the re-enactment of eye movement patterns that first occurred at viewing 9 (fixation reinstatement). To investigate these claims, we applied multivariate pattern analyses to 10 functional MRI (fMRI) and eye-tracking data collected while healthy human participants 11 repeatedly viewed and visualized complex images. We observed that the specificity of neural 12 reactivation correlated positively with vivid imagery and with memory for stimulus image 13 details. Moreover, neural reactivation correlated positively with fixation reinstatement, meaning 14 that image-specific eye movements accompanied image-specific patterns of brain activity during 15 visualization. These findings support the conception of mental imagery as a simulation of 16 perception, and provide evidence of the supportive role of eye-movement in neural reactivation. 17

Fixation reinstatement supports visuospatial memory in older adults.

“…It has been suggested that looking at nothing facilitates memory retrieval by reinstating the spatial index of the encoded image and its associated visual, linguistic, and conceptual features (Ferreira et al, 2008). In line with this proposal, a recent study using combined eyetracking-neuroimaging showed that both neural and eye movement activity patterns were reinstated during visualization and were correlated with each other (Bone at al., 2016). Although these findings advance a direct link between fixation reinstatement and internal memory representations, it remains unclear whether, and how, fixation reinstatement supports memory retrieval when internal representations are compromised, as may be the case in older adults.…”

Recurrence quantification analysis of eye movements during mental imagery

“…Moreover, interindividual differences in eye movement behavior were more pronounced during mental imagery than during perception. During perception, scene content remains visible, but during imagery, the imagined scene must be reactivated repeatedly since mental images do not persist and rather fade over time (Bone et al, 2017;De Beni et al, 2007;Farah, 1989;Kosslyn, 1994). This reactivation process leads to more recurrent fixations.…”

Neural correlates of subsequent memory-related gaze reinstatement

“…Indeed, guided or spontaneous gaze shifts to regions viewed during encoding (i.e., gaze reinstatement) have been proposed to support memory retrieval by reactivating the spatiotemporal encoding context (Wynn et al, 2019). In line with this proposal, recent work using concurrent eyetracking and fMRI has indicated that gaze reinstatement elicits patterns of neural activity typically associated with successful memory retrieval, including HPC activity (Ryals et al, 2015) and whole-brain neural reactivation (Bone et al, 2018). Critically however, these findings do not speak to the cognitive and neural processes at encoding that support the creation of functional scanpaths.…”

“…Specifically, when presented with a previously encoded stimulus, or a cue to retrieve a previously encoded stimulus from memory, humans (and non-human primates, see Sakon & Suzuki, 2019) spontaneously reproduce the scanpath enacted during encoding (i.e., gaze reinstatement), and this reinstatement is predictive of mnemonic performance across a variety of tasks (e.g., Damiano & Walther, 2019;Foulsham et al, 2012;Johansson & Johansson, 2013;Laeng, Bloem, D'Ascenzo, & Tommasi, 2014;Laeng & Teodorescu, 2002;Olsen, Chiew, Buchsbaum, & Ryan, 2014;Scholz, Mehlhorn, & Krems, 2016;Wynn, Olsen, Binns, Buchsbaum, & Ryan, 2018;Wynn, Ryan, & Buchsbaum, 2020; for review, see Wynn et al, 2019). While there is now considerable evidence supporting a link between gaze reinstatement (i.e., reinstatement of encoding gaze patterns during retrieval) and memory retrieval, investigations regarding the neural correlates of this effect are recent and few (see Bone et al, 2018;Ryals, Wang, Polnaszek, & Voss, 2015), and no study to date has investigated the patterns of neural activity at encoding that predict subsequent gaze reinstatement. Thus, to further elucidate the link between eye movements and memory at the neural level, the present study used concurrent eye movement monitoring and functional magnetic resonance imaging (fMRI) to investigate the neural mechanisms at encoding that predict functional gaze reinstatement (i.e., gaze reinstatement that supports mnemonic performance) at retrieval, in the vein of subsequent memory studies (e.g., Brewer, Zhao, Desmond, Glover, & Gabrieli, 1998;Wagner et al, 1998; for review, see Hannula & Duff, 2017).…”