Internally generated hippocampal sequences as a vantage point to probe future‐oriented cognition

Abstract

Information processing in the rodent hippocampus is fundamentally shaped by internally generated sequences (IGSs), expressed during two different network states: theta sequences, which repeat and reset at the ∼8 Hz theta rhythm associated with active behavior, and punctate sharp wave-ripple (SWR) sequences associated with wakeful rest or slow-wave sleep. A potpourri of diverse functional roles has been proposed for these IGSs, resulting in a fragmented conceptual landscape. Here, we advance a unitary view of IGSs, proposing that they reflect an inferential process that samples a policy from the animal's generative model, supported by hippocampus-specific priors. The same inference affords different cognitive functions when the animal is in distinct dynamical modes, associated with specific functional networks. Theta sequences arise when inference is coupled to the animal's action-perception cycle, supporting online spatial decisions, predictive processing, and episode encoding. SWR sequences arise when the animal is decoupled from the action-perception cycle and may support offline cognitive processing, such as memory consolidation, the prospective simulation of spatial trajectories, and imagination. We discuss the empirical bases of this proposal in relation to rodent studies and highlight how the proposed computational principles can shed light on the mechanisms of future-oriented cognition in humans.

Model-Based Approaches to Active Perception and Control

“…However, we have also discussed how some models do-or in other words, the possibility for internal (generative) models to temporarily detach from the current sensorimotor loop may afford representational functions, in a way that is not easy to reconcile with non-representational enactive theories [17,19,20]. Thus, while the different formalisms discussed here (e.g., with or without internal models) have different features, powers, and limitations, model-based solutions seem more suited to address the problem of detached cognition-or how living organisms can temporarily detach from the here-and-now, to implement (for example) future-oriented forms of cognition [128,135].…”

“…In short, dynamical patterns of neuronal activations that code for behavioural trajectories (i.e., sequence of place cells) are observed in the rodent hippocampus both when animals are actively engaged in overt spatial navigation, and when they are disengaged from the sensorimotor loop, e.g., when they sleep or groom after consuming a food-the latter depending on an internally-generated, spontaneous mode of neuronal processing that generally does not require external sensory inputs. Internally-generated sequences that mimic closely (albeit within different dynamical modes) neuronal activations observed during overt navigation have been proposed to be neuronal instantiations of internal models, which play multiple roles including memory consolidation and planning-thus illustrating a possible way the brain might reuse brain dynamics/internal models in a "dual mode", across overt and covert cognitive processes [132][133][134][135][136][137]. An intriguing neurobiological possibility is that the internal models that produce internally generated sequences are formed by exploiting pre-existing internal neuronal dynamics that are initially "meaningless", but acquire their "meaning" (e.g., code for a specific behavioural trajectory of the animal) through situated interaction, when the internal (spontaneous) and external dynamics become coupled [138].…”

How to Characterize the Function of a Brain Region

“…This conceptual polyhedron can be illustrated by one of the most studied parts of the brain, the hippocampus. It has been associated with different memory functions, such as episodic [23], autobiographical [24], explicit [25], contextual [26], or associative [27] memory, and also with several 'processes', including declarative [28] or incremental learning [29], recollection [30], encoding [31], retention [32], consolidation [33], novelty detection [34], binding [35], comparator [36], mismatch detection [37], pattern separation [38], and inferential processes [39]. Furthermore, the hippocampus has been associated with particular 'behavioral domains' and 'tasks' such as spatial navigation [40], spatial discrimination [41], scene imagination [42], prospection [43], and allocentric representation [44].…”

Value-based decisions involve sequential sampling from memory

“…We focused on hippocampal memory systems, because the act of comparing items seems to invite consideration of features that are not captured by a simple object-value association. Such a process is likely to involve memory retrieval, but also episodic simulation and prospection -all of which have been shown to depend on the hippocampus [19][20][21][22][23][24][25] . It is this memory-based constructive process that we hypothesized is positioned to supply evidence during deliberation.…”