Redundant representations are required to disambiguate simultaneously presented complex stimuli

• Published in: PLoS computational biology 2023-08, Vol.19 (8), p.e1011327-e1011327
• Main Authors: Johnston, W Jeffrey, Freedman, David J
• Format: Article
• Language: English
• Subjects: Artificial neural networks; Assignment problem; Auditory perception; Automobiles; Biology and Life Sciences; Brain; Charitable foundations; Complexity; Errors; Firing pattern; Information sources; Neural networks; Neurons; Pedestrian crossings; Physical Sciences; Psychological research; Receptive field; Representations; Sensory integration; Short term memory; Social Sciences; Stimuli; Stimuli (Psychology)
• ISSN: 1553-7358; 1553-734X; 1553-7358
• DOI: 10.1371/journal.pcbi.1011327

A pedestrian crossing a street during rush hour often looks and listens for potential danger. When they hear several different horns, they localize the cars that are honking and decide whether or not they need to modify their motor plan. How does the pedestrian use this auditory information to pick out the corresponding cars in visual space? The integration of distributed representations like these is called the assignment problem, and it must be solved to integrate distinct representations across but also within sensory modalities. Here, we identify and analyze a solution to the assignment problem: the representation of one or more common stimulus features in pairs of relevant brain regions-for example, estimates of the spatial position of cars are represented in both the visual and auditory systems. We characterize how the reliability of this solution depends on different features of the stimulus set (e.g., the size of the set and the complexity of the stimuli) and the details of the split representations (e.g., the precision of each stimulus representation and the amount of overlapping information). Next, we implement this solution in a biologically plausible receptive field code and show how constraints on the number of neurons and spikes used by the code force the brain to navigate a tradeoff between local and catastrophic errors. We show that, when many spikes and neurons are available, representing stimuli from a single sensory modality can be done more reliably across multiple brain regions, despite the risk of assignment errors. Finally, we show that a feedforward neural network can learn the optimal solution to the assignment problem, even when it receives inputs in two distinct representational formats. We also discuss relevant results on assignment errors from the human working memory literature and show that several key predictions of our theory already have support.