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

Abstract

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.

Keywords: Adaptive function; Decision-making; Hippocampus; Imagination; Learning; Memory; Prefrontal cortex; Simulation.

Figure 1. Overview of CRAMS

(A) CRAMS is initiated by response conflict, such as occurs when choices must be made between various options (i.e., decision-making). This conflict generates action plans that could be executed given the constraints of the environment (i.e., affordances). One action plan is covertly generated, leading in turn to covert retrieval of memory related to experiences that were similar to the simulated action in the current situation. The contents of covert retrieval constitute simulated action outcomes that are then evaluated relative to current goals, an “action-memory simulation.” This process of action generation, covert retrieval, and evaluation of the simulated outcome continues iteratively until the value of a simulation exceeds a threshold of proximity to the goal, at which point the cycle ends and the currently selected action is thus performed. (B) The number of CRAMS cycles that would be needed in a given situation is hypothesized to depend on three primary factors: familiarity, uncertainty, and environmental affordances. In highly familiar situations, situations with low uncertainty (i.e., high contrast among simulated outcomes), and when the environment affords few possible options, CRAMS proceeds for relatively few cycles before reaching a satisfactory selection. In contrast, in highly novel situations, situations with high uncertainty (i.e., low contrast among simulated outcomes), and when the environment affords many possible options, relatively more CRAMS cycles are required to systematically test many options before arriving at a selection.

Figure 2. Hypothesized functional neuroanatomy for CRAMS

Regions hypothesized to contribute to each portion of the CRAMS cycle are shown superimposed on medial and lateral views of the human brain. Response conflict initiates CRAMS, causing lateral PFC (green oval) to generate action plans that cue hippocampus (blue oval) to engage covert memory retrieval of relevant experience. Medial PFC (red oval) supports evaluation of the action-memory simulation by comparing the simulated outcome to current goals. This cycle is repeated for multiple generated actions until the goal threshold is reached (yellow diamond), at which point CRAMS terminates and motor systems (black oval) are engaged to perform the selected action. Putative contributions from other regions include inputs from striatum and amygdala to medial PFC that aid in goal maintenance and evaluation, as well as interactions between lateral PFC and frontopolar cortex that aid in maintenance of the outcomes that have already been simulated across time. Anatomical images adapted with permission from (Martin, 1996) (Permission pending).

Figure 3. CRAMS varies among environments based on the richness of options

(A) The standard VTE apparatus involves a choice point with two options. Rodents thus iteratively simulate the two options before choosing. Early in training, alternation between the two options is high because of high novelty and high uncertainty, whereas alternation decreases with training (Figure 1B). (B) Similar choice behavior occurs in a more complex environment such as an arena, although the number of options available at every moment is much higher. Iteration thus occurs continuously among many options. Previous experiences with the same arena and with similar arenas, objects, and situations leads to more distinction among the various options during simulation (indicated by darker versus lighter arrows) and thus more efficient testing of the various options via CRAMS. (C and D) Humans are faced with similar challenges at discrete choice points as well as in more complex environments, and we hypothesize that similar CRAMS mechanisms guide choices.

Figure 4. Similar mechanisms for exploration of cognitive and physical spaces

A depiction of the mental search involved in name recall given a face is provided in order to highlight that CRAMS could be as relevant for choices among mental possibilities as it is for choices among action possibilities. For instance, face-cued name recall can involve search among different places, events, and situations in which the person could have been encountered. Similar to choices encountered in a physical space, one can encounter constraints in choices and variability in novelty and uncertainty imposed by the “cognitive” environment that can dictate the number of logical options to be considered, as well as the amount of time required to converge on a solution. Thus, choices that are considered more purely “mental” than choices regarding how to act could nonetheless rely on similar CRAMS mechanisms.