Distributed Representations in Memory: Insights from Functional Brain Imaging

Abstract

Forging new memories for facts and events, holding critical details in mind on a moment-to-moment basis, and retrieving knowledge in the service of current goals all depend on a complex interplay between neural ensembles throughout the brain. Over the past decade, researchers have increasingly leveraged powerful analytical tools (e.g., multi-voxel pattern analysis) to decode the information represented within distributed fMRI activity patterns. In this review, we discuss how these methods can sensitively index neural representations of perceptual and semantic content, and how leverage on the engagement of distributed representations provides unique insights into distinct aspects of memory-guided behavior. We emphasize that, in addition to characterizing the contents of memories, analyses of distributed patterns shed light on the processes that influence how information is encoded, maintained, or retrieved, and thus inform memory theory. We conclude by highlighting open questions about memory that can be addressed through distributed pattern analyses.

Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval

“…Briefly, for every 500-ms temporal epoch, spaced every 100 ms (80% overlap), during the encoding and retrieval periods, we constructed a feature vector containing oscillatory power information from five frequency bands (theta, 3.5-8 Hz; alpha, [8][9][10][11][12] Hz; beta, 13-25 Hz; low gamma, 30-58 Hz; high gamma, 62-100 Hz) and from all electrode locations (SI Materials and Methods). We quantified reinstatement between every temporal epoch during encoding and retrieval by calculating the cosine similarity between feature vectors.…”

“…Previous studies that provide empiric support for neural reinstatement have not investigated the temporal dynamics mediating this process (11,12,17,19). We build upon these studies, as the intracranial recordings we use here enable us to examine neural reinstatement with high temporal precision across multiple frequency bands.…”

“…Empiric support for neural reinstatement has largely emerged from functional MRI (fMRI) studies that have used multivoxel pattern analysis (MVPA) (10)(11)(12). MVPA relies on classifying neural activity during retrieval to dissociate broad manipulations such as category or task that are present during encoding (13)(14)(15)(16).…”

Memory Retrieval in Mice and Men

“…Ben-Yakov et al rodent studies, is that retrieval entails reinstatement of brain activity that was elicited during encoding (Damasio 1989;McClelland et al 1995;reviewed in Buckner and Wheeler 2001;Rugg et al 2008;Danker and Anderson 2010;Rissman and Wagner 2012;Levy and Wagner 2013). Influential data-driven cognitive theories posited that the match between encoding and retrieval cues and between level of processing (e.g., in verbal memoranda) is pertinent for successful retrieval (Tulving and Thomson 1973;Morris et al 1977).…”

The Neural Basis of Vivid Memory Is Patterned on Perception

“…To examine and precisely quantify the extent to which perception and memory share the same neural machinery requires an experimental strategy that captures the two corresponding states in their representational totality, allowing for the possibility that complex and variegated perceptual episodesand the memories that reprise these episodes-emerge from the coordinated activity of distributed brain networks (Postle, 2006;Craik, 2002). In this study, we used fMRI and multivoxel pattern analysis (Rissman & Wagner, 2012;Chadwick, Hassabis, Weiskopf, & Maguire, 2010;OʼToole et al, 2007;Polyn, Natu, Cohen, & Norman, 2005;Hasson, Nir, Levy, Fuhrmann, & Malach, 2004;Strother et al, 2002;Haxby et al, 2001) to examine to what extent rich multimodal memories, when characterized in their totality as distributed patterns of neural activation, are neurophysiological simulacra of their perceptual counterparts.…”