The cost of efficiency in flexible neural representations

Working memory depends on the flexible representation of stimulus information in neural activity, which changes dynamically depending on task. Stimulus transformations are thought to be efficient in use of neural resources and optimal for task performance. However, these transformations are often opaque, and efficiency may conflict with optimal performance. Here we show that in a working memory task requiring selective recall of one of two stimuli based on a context cue, the prefrontal cortex of two male monkeys prioritized efficiency by overwriting information within a shared neural subspace rather than maintaining distinct subspaces for each stimulus. In neural activity and recurrent neural networks such efficiency incurs a cost, in that efficient representations are more prone to errors. Conversely, stimulation of the cholinergic forebrain which improves behavior altered this default mechanism by encoding distinct contexts in higher dimensions. These findings demonstrate a fundamental tradeoff between efficiency and effectiveness in flexibly updating working memory.