Large-scale neuronal recording techniques have enabled discoveries of population-level mechanisms for neural computation. However, it is not clear how these mechanisms form by trial-and-error learning. In this article, we present an initial effort to characterize the population activity in monkey prefrontal cortex (PFC) and hippocampus (HPC) during the learning phase of a paired-associate task. To analyze the population data, we introduce the normalized distance, a dimensionless metric that describes the encoding of cognitive variables from the geometrical relationship among neural trajectories in state space. It is found that PFC exhibits a more sustained encoding of the visual stimuli, whereas HPC only transiently encodes the identity of the associate stimuli. Surprisingly, after learning, the neural activity is not reorganized to reflect the task structure, raising the possibility that learning is accompanied by some “silent” mechanism that does not explicitly change the neural representations. We did find partial evidence on the learning-dependent changes for some of the task variables. This study shows the feasibility of using normalized distance as a metric to characterize and compare population-level encoding of task variables and suggests further directions to explore learning-dependent changes in the neural circuits.

Behavioral research in human verbal memory function led to the initial definition of episodic memory and semantic memory. A complete model of the neural mechanisms of episodic memory must include the capacity to encode and mentally reconstruct everything that humans can recall from their experience. This article proposes new model features necessary to address the complexity of episodic memory encoding and recall in the context of broader cognition and the functional properties of neurons that could contribute to this broader scope of memory. Many episodic memory models represent individual snapshots of the world with a sequence of vectors, but a full model must represent complex functions encoding and retrieving the relations between multiple stimulus features across space and time on multiple hierarchical scales. Episodic memory involves not only the space and time of an agent experiencing events within an episode but also features shown in neurophysiological data such as coding of speed, direction, boundaries, and objects. Episodic memory includes not only a spatio-temporal trajectory of a single agent but also segments of spatio-temporal trajectories for other agents and objects encountered in the environment consistent with data on encoding the position and angle of sensory features of objects and boundaries. We will discuss potential interactions of episodic memory circuits in the hippocampus and entorhinal cortex with distributed neocortical circuits that must represent all features of human cognition.

Many behavioral tasks require goal-directed actions to obtain delayed reward. The prefrontal cortex appears to mediate many aspects of goal-directed decision making. This article presents a model of prefrontal cortex function emphasizing the influence of goal-related activity on the choice of the next motor output. The model can be interpreted in terms of key elements of Reinforcement Learning Theory. Different neocortical minicolumns represent distinct sensory input states and distinct motor output actions. The dynamics of each minicolumn include separate phases of encoding and retrieval. During encoding, strengthening of excitatory connections forms forward and reverse associations between each state, the following action, and a subsequent state, which may include reward. During retrieval, activity spreads from reward states throughout the network. The interaction of this spreading activity with a specific input state directs selection of the next appropriate action. Simulations demonstrate how these mechanisms can guide performance in a range of goal-directed tasks, and provide a functional framework for some of the neuronal responses previously observed in the medial prefrontal cortex during performance of spatial memory tasks in rats.