Human hippocampal theta oscillations reflect sequential dependencies during spatial planning

Kaplan, Raphael; Campo, Adrià Tauste; Bush, Daniel; King, John A.; Príncipe, Alessandro; Köster, Raphael; Ley-Nacher, Miguel; Rocamora, Rodrigo; Friston, Karl J.

doi:10.1101/372011

Cited by 4 publications

(4 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Theta sequences have yet to be directly studied during a multi-step planning task, therefore it is currently unknown how these mechanisms extend to planning over multiple steps. However, a recent study [100] demonstrated increased theta power in humans during multi-step spatial planning, consistent with the idea that theta sequences might be involved in this process.…”

Section: Hippocampal Sequences and Multi-step Planningsupporting

confidence: 73%

Multi-step planning in the brain

Miller

Venditto

2021

Current Opinion in Behavioral Sciences

View full text Add to dashboard Cite

Decisions in the natural world are rarely made in isolation. Each action that an organism selects will affect the future situations in which it finds itself, and those situations will in turn affect the future actions that are available. Achieving real-world goals often requires successfully navigating a sequence of many actions. An efficient and flexible way to achieve such goals is to construct an internal model of the environment, and use it to plan behavior multiple steps into the future. This process is known as multi-step planning, and its neural mechanisms are only beginning to be understood. Here, we review recent advances in our understanding of these mechanisms, many of which take advantage of multi-step decision tasks for humans and animals. Multi-Step Planning Shares Neural Mechanisms with Associative Learning Work on the neural mechanisms of planning builds upon a rich body of work investigating cognitive capacities upon which planning may depend. One of these is the ability to associate stimuli or actions with specific expected outcomes (e.g. walk south → arrive at lab; walk north → arrive at coffee shop). Behavior guided by such outcome-specific associations can be thought of as exercising a simple one-step form of planning. Researchers have developed several selective assays of this capacity and have used them extensively to identify and characterize the neural structures that support outcome-specific associations [23]. A second cognitive capacity necessary for multi-step planning is "inference": the ability to combine separately-learned associations in order to form new associations between items that may never have been encountered together before (e.g. walk north → arrive at coffee shop; place order → receive coffee; ∴ to obtain coffee, walk north). Researchers have developed assays of this capacity as well, and have used them to identify neural structures necessary for combining separately-learned associations [e.g. 24,25,26]. Mechanisms for outcome-specific associations and for inference are universally present in theoretical accounts of multi-step planning (see box). Recent work has borne out the idea that the neural structures which support outcome-specific associations and inference in associative learning tasks likely support planning in multi-step decision tasks as well. Orbitofrontal Cortex and Model-Based Prediction Regions of frontal cortex belonging to the orbital network (especially areas LO and AIv in rodents and areas 13 and 11l in primates, often referred to as "OFC" or "lateral OFC") play an important role both in outcome-specific associations and in inference. Lesions or inactivations of OFC have been shown to impair performance on behavioral assays of these capacities in rodents [27-29] and to impair use of outcome-specific associations in nonhuman primates [30]. Recent data have extended these findings to humans as well, showing that disruption of OFC activity impairs performance on assays of outcome-specific associations and of inference [31,32]. Correspondingly, neural acti...

show abstract

Section: Hippocampal Sequences and Multi-step Planningsupporting

confidence: 73%

Multi-step planning in the brain

Miller

Venditto

2021

Current Opinion in Behavioral Sciences

View full text Add to dashboard Cite

show abstract

“…Our evidence for on-task replay relates to research in rodents, where time-compressed sequential place cell activations, called theta sequences, occur during active behavior (Foster and Wilson, 2007) and reflect multiple potential future trajectories when the animal pauses at a decision point (Johnson and Redish, 2007), or cycle between future trajectories during movement (Kay et al, 2020) possibly reflecting an online planning process. Similar relationships between hippocampal theta and planning have been observed in human magnetoencephalography (MEG) experiments (Kaplan et al, 2020), which have also yielded evidence for on-task planning in the form of fast sequential neural reactivation (Kurth-Nelson et al, 2016; Eldar et al, 2020). An fMRI study in humans has related on-task prospective neural activation to model-based decision-making (Doll et al, 2015), but the temporal dynamics of the prospective neural representations remained unclear.…”

Section: Discussionsupporting

confidence: 60%

Statistical learning of successor representations is related to on-task replay

Wittkuhn

Krippner

2022

Preprint

View full text Add to dashboard Cite

Humans automatically infer higher-order relationships between events in the environment from their statistical co-occurrence, often without conscious awareness. Neural replay of task representations, which has been described as sampling from a learned transition structure of the environment, is a candidate mechanism by which the brain could use or even learn such relational information in the service of adaptive behavior. Human participants viewed sequences of images that followed probabilistic transitions determined by ring-like graph structures. Behavioral modeling revealed that participants acquired multi-step transition knowledge through gradual updating of an internal successor representation (SR) model, although half of participants did not indicate any knowledge about the sequential task structure. To investigate neural replay, we analyzed dynamics of multivariate functional magnetic resonance imaging (fMRI) patterns during short pauses from the ongoing statistical learning task. Evidence for sequential replay consistent with the probabilistic task structure was found in occipito-temporal and sensorimotor cortices during short on-task intervals. These findings indicate that implicit learning of higher-order relationships establishes an internal SR-based map of the task, and is accompanied by cortical on-task replay.

show abstract

“…In humans the hippocampus is involved in both episodic memory processes and thinking about the future (Schacter et al, 2007), and theta sequences may therefore have a fundamental role in these processes Jaramillo & Kempter, 2017;Terada et al, 2017;Wang et al, 2015). In support of this hypothesis, the developmental emergence of theta sequences coincides with the maturation of hippocampal memory (Muessig et al, 2019), and increases in hippocampal theta power have been observed in humans undertaking sequential planning tasks (Kaplan et al, 2020).…”

Section: ……Figure 7 Here……………………………………………………………………………mentioning

confidence: 87%