Biology subjects

Whittington, J. C. R.

Publications and source records attributed to Whittington, J. C. R..

4 recordsLinked to original sources

bioRxiv2023

On prefrontal working memory and hippocampal episodic memory: Unifying memories stored in weights and activation slots

Remembering events in the past is crucial to intelligent behaviour. Flexible memory retrieval, beyond simple recall, requires a cognitive map, or model of how sensations, actions, and latent environmental or task states are all related to one another. Two key brain systems are implicated in this process: the hippocampal episodic memory (EM) system and the prefrontal working memory (WM) system. While an understanding of the hippocampal system, from computation to algorithm and representation, is emerging, less is understood about how the prefrontal WM system can give rise to flexible computations beyond simple memory retrieval, and even less is understood about how the two systems relate to each other. Here we develop a mathematical theory relating the algorithms and representations of EM and WM by unveiling a duality between storing memories in synapses versus neural activity. In doing so, we develop a formal theory of the algorithms and representations of prefrontal WM in terms of structured, and controllable, neural subspaces (termed activity slots) that together can represent a dynamic cognitive map without any need for synaptic plasticity. By building models using this formalism, we elucidate the differences, similarities, and trade-offs between the hippocampal and prefrontal algorithms. Lastly, we show that several prefrontal representations in tasks ranging from list learning to cue dependent recall are unified as controllable activity slots. Our results unify frontal and temporal representations of memory, and offer a new basis for understanding dynamic prefrontal representations of WM.

neuroscience↗

bioRxiv2023

Constructing future behaviour in the hippocampal formation through composition and replay

Hippocampus is critical for memory, imagination and constructive reasoning. However, recent models have suggested that its neuronal responses can be well explained by graphs, or state-spaces, that model the transitions between experiences. Here we use simulations and hippocampal recordings to reconcile these views. We show that if state-spaces are constructed compositionally from existing building blocks, or primitives, hippocampal responses can be interpreted as compositional memories, binding these primitives together. Critically, this enables agents to behave optimally in novel environments with no new learning, inferring behaviour directly from the composition. We predict a role for hippocampal replay in building and consolidating these compositional memories. Importantly, due to their compositional nature, replay can construct states the agent has never experienced - effectively building memories of the future. We test these predictions in two datasets by showing that replay events from newly discovered landmarks induce and strengthen new remote firing fields. These memories, built in replay, are compositional. When the landmark is moved, replay builds a new firing field at the same vector to the new location. Together, these findings provide a framework for reasoning about compositional memories, and demonstrate that such memories are formed in hippocampal replay.

neuroscience↗

bioRxiv2018

Intuitive planning: global navigation through cognitive maps based on grid-like codes

It is proposed that a cognitive map encoding the relationships between objects supports the ability to flexibly navigate the world. Place cells and grid cells provide evidence for such a map in a spatial context. Emerging evidence suggests analogous cells code for non-spatial information. Further, it has been shown that grid cells resemble the eigenvectors of the relationship between place cells and can be learnt from local inputs. Here we show that these locally-learnt eigenvectors contain not only local information but also global knowledge that can provide both distributions over future states as well as a global distance measure encoding approximate distances between every object in the world. By simply changing the weights in the grid cell population, it is possible to switch between computing these different measures. We demonstrate a simple algorithm can use these measures to globally navigate arbitrary topologies without searching more than one step ahead. We refer to this as intuitive planning.

neuroscience↗

bioRxiv2018

What is a cognitive map? Organising knowledge for flexible behaviour

It is proposed that a cognitive map encoding the relationships between entities in the world supports flexible behaviour, but the majority of the neural evidence for such a system comes from studies of spatial navigation. Recent work describing neuronal parallels between spatial and non-spatial behaviours has rekindled the notion of a systematic organisation of knowledge across multiple domains. We review experimental evidence and theoretical frameworks that point to principles unifying these apparently disparate functions. These principles describe how to learn and use abstract, generalisable knowledge and suggest map-like representations observed in a spatial context may be an instance of general coding mechanisms capable of organising knowledge of all kinds. We highlight how artificial agents endowed with such principles exhibit flexible behaviour and learn map-like representations observed in the brain. Finally, we speculate on how these principles may offer insight into the extreme generalisations, abstractions and inferences that characterise human cognition.

neuroscience↗