Independent Continuous Tracking of Multiple Agents in the Human Hippocampus

Abstract

The pursuit of fleeing prey is a core element of many species behavioral repertoires. It poses the difficult problem of continuous tracking of multiple agents, including both self and others. To understand how this tracking is implemented neurally, we examined responses of hippocampal neurons while humans performed a joystick-controlled continuous prey-pursuit task involving two simultaneously fleeing prey (and, in some cases, a predator) in a virtual open field. We found neural maps encoding the positions of all the agents. All maps were multiplexed in single neurons and were disambiguated by the use of the population coding principle of semi-orthogonal subspaces, which can facilitate cross-agent generalization. Some neurons, more common in the posterior hippocampus, had narrow tuning functions reminiscent of place cells, lower firing rates, and high information per spike; others, which were found in both anterior and posterior hippocampus, had broad tuning functions, higher firing rates, and less information per spike. Semi-orthogonalization was selectively associated with the broadly tuned neurons. These results suggest an answer to the problem of navigational individuation, that is, how mapping codes can distinguish different agents, and establish the neuronavigational foundations of pursuit.