Information theoretic measures of neural and behavioural coupling predict representational drift

In many parts of the brain, population tuning to stimuli and behaviour gradually changes over the course of days to weeks in a phenomenon known as representational drift. The tuning stability of individual cells varies over the population, and it remains unclear what drives this heterogeneity. We investigate how a neuron’s tuning stability relates to its shared variability with other neurons in the population using two published datasets from posterior parietal cortex and visual cortex. We quantified the contribution of pairwise interactions to behaviour or stimulus encoding by partial information decomposition, which breaks down the mutual information between the pairwise neural activity and the external variable into components uniquely provided by each neuron and by their interactions. Information shared by the two neurons is termed ‘redundant’, and information requiring knowledge of the state of both neurons is termed ‘synergistic’. We found that a neuron’s tuning stability is positively correlated with the strength of its average pairwise redundancy with the population. We hypothesize that subpopulations of neurons show greater stability because they are tuned to salient features common across multiple tasks. Regardless of the mechanistic implications of our work, the stability–redundancy relationship may support improved longitudinal neural decoding in technology that has to track population dynamics over time, such as brain–machine interfaces.Author summary: Activity in the brain represents information about the outside world and how we interact with it. Recent evidence shows that these representations slowly change day to day, while memories and learned behaviours stay stable. Individual neurons change their relationship to external variables at different rates, and we explore how interactions with other neurons in the population relates to this neuron-to-neuron variability. We find that more stable neurons tend to share information about external variables with many other neurons. Our results suggest there are constraints on how representations can change over time, and that these constraints are exhibited in shared fluctuations in activity among neurons in the population.