Detailed Episodic Memory Depends on Concurrent Reactivation of Basic Visual Features within the Posterior Hippocampus and Early Visual Cortex.

The hippocampus is a key brain region for the storage and retrieval of episodic memories, but how it performs this function is unresolved. Leading theories posit that the hippocampus stores a sparse representation, or "index," of the pattern of neocortical activity that occurred during perception. During retrieval, reactivation of the index by a partial cue facilitates the reactivation of the associated neocortical pattern. Therefore, episodic retrieval requires joint reactivation of the hippocampal index and the associated neocortical networks. To test this theory, we examine the relation between performance on a recognition memory task requiring retrieval of image-specific visual details and feature-specific reactivation within the hippocampus and neocortex. We show that trial-by-trial recognition accuracy correlates with neural reactivation of low-level features (e.g., luminosity and edges) within the posterior hippocampus and early visual cortex for participants with high recognition lure accuracy. As predicted, the two regions interact, such that recognition accuracy correlates with hippocampal reactivation only when reactivation co-occurs within the early visual cortex (and vice versa). In addition to supporting leading theories of hippocampal function, our findings show large individual differences in the features underlying visual memory and suggest that the anterior and posterior hippocampus represents gist-like and detailed features, respectively.

Feature-specific neural reactivation during episodic memory.

We present a multi-voxel analytical approach, feature-specific informational connectivity (FSIC), that leverages hierarchical representations from a neural network to decode neural reactivation in fMRI data collected while participants performed an episodic visual recall task. We show that neural reactivation associated with low-level (e.g. edges), high-level (e.g. facial features), and semantic (e.g. "terrier") features occur throughout the dorsal and ventral visual streams and extend into the frontal cortex. Moreover, we show that reactivation of both low- and high-level features correlate with the vividness of the memory, whereas only reactivation of low-level features correlates with recognition accuracy when the lure and target images are semantically similar. In addition to demonstrating the utility of FSIC for mapping feature-specific reactivation, these findings resolve the contributions of low- and high-level features to the vividness of visual memories and challenge a strict interpretation the posterior-to-anterior visual hierarchy.

Eye Movement Reinstatement and Neural Reactivation During Mental Imagery.

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

Selective scanpath repetition during memory-guided visual search.

Visual search efficiency improves with repetition of a search display, yet the mechanisms behind these processing gains remain unclear. According to Scanpath Theory, memory retrieval is mediated by repetition of the pattern of eye movements or "scanpath" elicited during stimulus encoding. Using this framework, we tested the prediction that scanpath recapitulation reflects relational memory guidance during repeated search events. Younger and older subjects were instructed to find changing targets within flickering naturalistic scenes. Search efficiency (search time, number of fixations, fixation duration) and scanpath similarity (repetition) were compared across age groups for novel (V1) and repeated (V2) search events. Younger adults outperformed older adults on all efficiency measures at both V1 and V2, while the search time benefit for repeated viewing (V1-V2) did not differ by age. Fixation-binned scanpath similarity analyses revealed repetition of initial and final (but not middle) V1 fixations at V2, with older adults repeating more initial V1 fixations than young adults. In young adults only, early scanpath similarity correlated negatively with search time at test, indicating increased efficiency, whereas the similarity of V2 fixations to middle V1 fixations predicted poor search performance. We conclude that scanpath compression mediates increased search efficiency by selectively recapitulating encoding fixations that provide goal-relevant input. Extending Scanpath Theory, results suggest that scanpath repetition varies as a function of time and memory integrity.