Spatial Learning and Action Planning in a Prefrontal Cortical Network Model

The interplay between hippocampus and prefrontal cortex (PFC) is fundamental to spatial cognition. Complementing hippocampal place coding, prefrontal representations provide more abstract and hierarchically organized memories suitable for decision making. We model a prefrontal network mediating distributed information processing for spatial learning and action planning. Specific connectivity and synaptic adaptation principles shape the recurrent dynamics of the network arranged in cortical minicolumns. We show how the PFC columnar organization is suitable for learning sparse topological-metrical representations from redundant hippocampal inputs. The recurrent nature of the network supports multilevel spatial processing, allowing structural features of the environment to be encoded. An activation diffusion mechanism spreads the neural activity through the column population leading to trajectory planning. The model provides a functional framework for interpreting the activity of PFC neurons recorded during navigation tasks. We illustrate the link from single unit activity to behavioral responses. The results suggest plausible neural mechanisms subserving the cognitive “insight” capability originally attributed to rodents by Tolman & Honzik. Our time course analysis of neural responses shows how the interaction between hippocampus and PFC can yield the encoding of manifold information pertinent to spatial planning, including prospective coding and distance-to-goal correlates. Author Summary: We study spatial cognition, a high-level brain function based upon the ability to elaborate mental representations of the environment supporting goal-oriented navigation. Spatial cognition involves parallel information processing across a distributed network of interrelated brain regions. Depending on the complexity of the spatial navigation task, different neural circuits may be primarily involved, corresponding to different behavioral strategies. Navigation planning, one of the most flexible strategies, is based on the ability to prospectively evaluate alternative sequences of actions in order to infer optimal trajectories to a goal. The hippocampal formation and the prefrontal cortex are two neural substrates likely involved in navigation planning. We adopt a computational modeling approach to show how the interactions between these two brain areas may lead to learning of topological representations suitable to mediate action planning. Our model suggests plausible neural mechanisms subserving the cognitive spatial capabilities attributed to rodents. We provide a functional framework for interpreting the activity of prefrontal and hippocampal neurons recorded during navigation tasks. Akin to integrative neuroscience approaches, we illustrate the link from single unit activity to behavioral responses while solving spatial learning tasks.