We argue that neural representations of memories are best thought of as spatially transformed versions of perceptual representations

Transforming the Concept of Memory Reactivation. Serra E. Favila, Hongmi Lee, Brice A. Kuhl. Trends in Neurosciences, October 8 2020. https://doi.org/10.1016/j.tins.2020.09.006

Highlights

.  A foundational finding in the field of memory is that content-sensitive patterns of neural activity expressed during perceptual experiences are re-expressed when experiences are remembered, a phenomenon termed reactivation. However, reactivation obscures key differences in how perceptual events and memories are represented in the brain.

.  Recent findings suggest systematic, spatial transformations of content-sensitive neural activity patterns from perception to memory retrieval. These transformations occur within sensory cortex and from sensory cortex to frontoparietal cortex.

.  We consider why spatial transformations occur and identify critical questions to be addressed in future research. Understanding the ways in which memory representations differ from perceptual representations will critically inform theoretical accounts of memory and will help clarify how the brain recreates the past.

Abstract: Reactivation refers to the phenomenon wherein patterns of neural activity expressed during perceptual experience are re-expressed at a later time, a putative neural marker of memory. Reactivation of perceptual content has been observed across many cortical areas and correlates with objective and subjective expressions of memory in humans. However, because reactivation emphasizes similarities between perceptual and memory-based representations, it obscures differences in how perceptual events and memories are represented. Here, we highlight recent evidence of systematic differences in how (and where) perceptual events and memories are represented in the brain. We argue that neural representations of memories are best thought of as spatially transformed versions of perceptual representations. We consider why spatial transformations occur and identify critical questions for future research.

Keywords: episodic memoryreactivationreinstatementmemory transformationsensory cortexfrontoparietal cortex

Outstanding Questions

To what extent do changes in information content account for spatial transformation from perception to retrieval? Are certain stimulus features that are present during perception systematically lost or distorted in memory? Do memory representations gain information that is absent or weakly present during perception through integration with other memories or existing knowledge structures (schemas)?

What determines the relative degree of neural reactivation versus transformation across brain regions observed during memory retrieval? For example, is greater transformation observed when memory tasks promote conceptual processing at retrieval? Conversely, is relatively greater reactivation in sensory areas observed when memory tasks promote perceptual processing? Does the relative degree of reactivation versus transformation depend on whether memory tasks involve recall versus recognition judgments? Do reactivation and transformation trade-off or are they independent?

Does the degree of transformation across brain regions depend on the temporal lag between perception and memory retrieval? Transformation potentially occurs in working memory paradigms with delays on the order of seconds, yet there is also considerable work documenting consolidation-related transformations at timescales of hours to years. What are the similarities and differences between transformations that occur across these vastly different timescales?

What is the relationship between transformation within sensory areas and transformation from sensory to frontoparietal regions? These two forms of transformation have been studied separately to date and it is thus unclear whether they are related and, if so, how. Notably, the frontoparietal and sensory regions that exhibit biases toward memory-based representations are functionally connected with the hippocampus. To what extent can connectivity with the hippocampus explain both sets of findings?