Representation of viewed and recalled film clips in patterns of brain activity in a person with developmental amnesia

Abstract

As clear memories transport us back into the past, the brain also revives prior patterns of neural activity, a phenomenon known as neural reactivation. While growing evidence indicates a link between neural reactivation and typical variations in memory performance in healthy individuals, it is unclear how and to what extent reactivation is disrupted by a memory disorder. The current study characterizes neural reactivation in a case of amnesia using Multivoxel Pattern Analysis (MVPA). We tested NC, an individual with developmental amnesia linked to a diencephalic stroke, and 19 young adult controls on a functional magnetic resonance imaging (fMRI) task during which participants viewed and recalled short videos multiple times. An encoding classifier trained and tested to identify videos based on brain activity patterns elicited at perception revealed superior classification in NC. The enhanced consistency in stimulus representation we observed in NC at encoding was accompanied by an absence of multivariate repetition suppression, which occurred over repeated viewing in the controls. Another recall classifier trained and tested to identify videos during mental replay indicated normal levels of classification in NC, despite his poor memory for stimulus content. However, a cross-condition classifier trained on perception trials and tested on mental replay trials—a strict test of reactivation—revealed significantly poorer classification in NC. Thus, while NC's brain activity was consistent and stimulus-specific during mental replay, this specificity did not reflect the reactivation of patterns elicited at perception to the same extent as controls. Fittingly, we identified brain regions for which activity supported stimulus representation during mental replay to a greater extent in NC than in controls. This activity was not modeled on perception, suggesting that compensatory patterns of representation based on generic knowledge can support consistent mental constructs when memory is faulty. Our results reveal several ways in which amnesia impacts distributed patterns of stimulus representation during encoding and retrieval.