A Roadmap for Understanding Memory: Decomposing Cognitive Processes into Operations and Representations

Thanks to patients Phineas Gage and Henry Molaison, we have long known that behavioral control depends on the frontal lobes, whereas declarative memory depends on the medial temporal lobes (MTL). For decades, cognitive functions—behavioral control, declarative memory—have served as labels for characterizing the division of labor in cortex. This approach has made enormous contributions to understanding how the brain enables the mind, providing a systems-level explanation of brain function that constrains lower-level investigations of neural mechanism. Today, the approach has evolved such that functional labels are often applied to brain networks rather than focal brain regions. Furthermore, the labels have diversified to include both broadly-defined cognitive functions (declarative memory, visual perception) and more circumscribed mental processes (recollection, familiarity, priming). We ask whether a process—a high-level mental phenomenon corresponding to an introspectively-identifiable cognitive event—is the most productive label for dissecting memory. For example, recollection conflates a neurocomputational operation (pattern completion-based retrieval) with a class of representational content (associative, high-dimensional memories). Because a full theory of memory must identify operations and representations separately, and specify how they interact, we argue that processes like recollection constitute inadequate labels for characterizing neural mechanisms. Instead, we advocate considering the component operations and representations of processes like recollection in isolation. For the organization of memory, the evidence suggests that pattern completion is recapitulated widely across the ventral visual stream and MTL, but the division of labor between sites within this pathway can be explained by representational content.