Recurrent predictive coding models for associative memory employing covariance learning

Mufeng Tang, Tommaso Salvatori, Beren Millidge, Yuhang Song, Thomas Lukasiewicz and Rafal Bogacz

PLOS Computational Biology, 2023, vol. 19, issue 4, 1-27

Abstract: The computational principles adopted by the hippocampus in associative memory (AM) tasks have been one of the most studied topics in computational and theoretical neuroscience. Recent theories suggested that AM and the predictive activities of the hippocampus could be described within a unitary account, and that predictive coding underlies the computations supporting AM in the hippocampus. Following this theory, a computational model based on classical hierarchical predictive networks was proposed and was shown to perform well in various AM tasks. However, this fully hierarchical model did not incorporate recurrent connections, an architectural component of the CA3 region of the hippocampus that is crucial for AM. This makes the structure of the model inconsistent with the known connectivity of CA3 and classical recurrent models such as Hopfield Networks, which learn the covariance of inputs through their recurrent connections to perform AM. Earlier PC models that learn the covariance information of inputs explicitly via recurrent connections seem to be a solution to these issues. Here, we show that although these models can perform AM, they do it in an implausible and numerically unstable way. Instead, we propose alternatives to these earlier covariance-learning predictive coding networks, which learn the covariance information implicitly and plausibly, and can use dendritic structures to encode prediction errors. We show analytically that our proposed models are perfectly equivalent to the earlier predictive coding model learning covariance explicitly, and encounter no numerical issues when performing AM tasks in practice. We further show that our models can be combined with hierarchical predictive coding networks to model the hippocampo-neocortical interactions. Our models provide a biologically plausible approach to modelling the hippocampal network, pointing to a potential computational mechanism during hippocampal memory formation and recall, which employs both predictive coding and covariance learning based on the recurrent network structure of the hippocampus.Author summary: The hippocampus and adjacent cortical areas have long been considered essential for the formation of associative memories. It has been recently suggested that the hippocampus stores and retrieves memory by generating predictions of ongoing sensory inputs. Computational models have thus been proposed to account for this predictive nature of the hippocampal network during associative memory using predictive coding, a general theory of information processing in the cortex. However, these hierarchical predictive coding models of the hippocampus did not take into account important hippocampal architectural components that may store statistical regularities supporting associative memory, which also hinders a unified view with classical models learning these regularities. To address these issues, here we present a family of predictive coding models that also learn the statistical information needed for associative memory. Our models can stably perform associative memory tasks in a biologically plausible manner, even with large structured data such as natural scenes. Our work provides a possible mechanism of how the recurrent hippocampal network may employ various computational principles concurrently to perform associative memory.

Date: 2023
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pcbi00:1010719

DOI: 10.1371/journal.pcbi.1010719

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