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. Understanding the world and making optimal decisions requires using the most relevant information while at the same time ignoring irrelevant information, a psychological phenomenon known as “cognitive control.” How the same population of neurons deals with multiple streams of information simultaneously is poorly understood. In this study, we investigated the underlying neural mechanisms of cognitive control in a network of hippocampal neurons known to represent space. We implanted electrodes into the hippocampus of rats and recorded the action potential discharge of many neurons at the same time. The recordings were made while rats that were foraging on a rotating disk used cognitive control to coordinate spatial information from different spatial frames. We found that at each moment, discharge preferentially represented location in one or the other spatial frame. Importantly, we were able to influence the behavioral relevance of these spatial frames, and we found that discharge alternated between signaling location in one or the other frames in accord with its current behavioral importance. The timing of when these neurons were active was also related to their function, such that neurons collectively represented locations in the same spatial frame if they were coactive within a few tens of milliseconds to seconds. We conclude that cognitive control is mediated by a dynamic functional grouping. Neural activity distributed across many neurons transiently organizes into functional groups by coactive firing that represents a coherent stream of information.