Covert rapid action-memory simulation (CRAMS): A hypothesis of hippocampal-prefrontal interactions for adaptive behavior

Effective choices generally require memory, yet little is known regarding the cognitive or neural mechanisms that allow memory to influence choices. We outline a new framework proposing that covert memory processing of hippocampus interacts with action-generation processing of prefrontal cortex in order to arrive at optimal, memory-guided choices. Covert, rapid action-memory simulation (CRAMS) is proposed here as a framework for understanding cognitive and/or behavioral choices, whereby prefrontal-hippocampal interactions quickly provide multiple simulations of potential outcomes used to evaluate the set of possible choices. We hypothesize that this CRAMS process is automatic, obligatory, and covert, meaning that many cycles of action-memory simulation occur in response to choice conflict without an individual's necessary intention and generally without awareness of the simulations, leading to adaptive behavior with little perceived effort. CRAMS is thus distinct from influential proposals that adaptive memory-based behavior in humans requires consciously experienced memory-based construction of possible future scenarios and deliberate decisions among possible future constructions. CRAMS provides an account of why hippocampus has been shown to make critical contributions to the short-term control of behavior, and it motivates several new experimental approaches and hypotheses that could be used to better understand the ubiquitous role of prefrontal-hippocampal interactions in situations that require adaptively using memory to guide choices. Importantly, this framework provides a perspective that allows for testing decision-making mechanisms in a manner that translates well across human and nonhuman animal model systems.