Optimal Dynamic Coding by Mixed-Dimensionality Neurons in the Head-Direction System of Bats

Ethologically relevant stimuli are often multidimensional. In many brain systems, neurons with “pure” tuning to one stimulus dimension are found along with “conjunctive” neurons that encode several dimensions, forming an apparently redundant representation. Here we show using theoretical analysis that a mixed-dimensionality code can efficiently represent a stimulus in different behavioral regimes: encoding by conjunctive cells is more robust when the stimulus changes quickly, whereas on long timescales pure cells represent the stimulus more efficiently with fewer neurons. We tested our predictions experimentally in the bat head-direction system and found that many head-direction cells switched their tuning dynamically from pure to conjunctive representation as a function of angular velocity—confirming our theoretical prediction. More broadly, our results suggest that optimal dimensionality depends on population size and on the time available for decoding—which might explain why mixed-dimensionality representations are common in sensory, motor, and higher cognitive systems across species.