Dynamic Grouping of Hippocampal Neural Activity During Cognitive Control of Two Spatial Frames

Cognitive control is the ability to coordinate multiple streams of information to prevent confusion and select appropriate behavioral responses, especially when presented with competing alternatives. Despite its theoretical and clinical significance, the neural mechanisms of cognitive control are poorly understood. Using a two-frame place avoidance task and partial hippocampal inactivation, we confirmed that intact hippocampal function is necessary for coordinating two streams of spatial information. Rats were placed on a continuously rotating arena and trained to organize their behavior according to two concurrently relevant spatial frames: one stationary, the other rotating. We then studied how information about locations in these two spatial frames is organized in the action potential discharge of ensembles of hippocampal cells. Both streams of information were represented in neuronal discharge—place cell activity was organized according to both spatial frames, but almost all cells preferentially represented locations in one of the two spatial frames. At any given time, most coactive cells tended to represent locations in the same spatial frame, reducing the risk of interference between the two information streams. An ensemble's preference to represent locations in one or the other spatial frame alternated within a session, but at each moment, location in the more behaviorally relevant spatial frame was more likely to be represented. This discharge organized into transient groups of coactive neurons that fired together within 25 ms to represent locations in the same spatial frame. These findings show that dynamic grouping, the transient coactivation of neural subpopulations that represent the same stream of information, can coordinate representations of concurrent information streams and avoid confusion, demonstrating neural-ensemble correlates of cognitive control in hippocampus.