Prefrontal Cortex and Basal Ganglia Attributes Underlying Behavioral Flexibility

Abstract

The Kesner neurobiologically based attribute model of memory is a multiple memory systems model proposing that different brain systems support specific memory representations based on attribute information. The model has served as a useful framework to test hypotheses about the nature of memory representations in the brain. The model has expanded beyond the neurobiology of memory to investigate how separate prefrontal cortex subregions support behavioral flexibility based on how attribute information must be used in different ways to allow adaptive behavior. Behavioral flexibility refers to the ability to adapt strategies or choice patterns when changes in external or internal conditions signal a behavioral strategy switch. The chapter first describes how different prefrontal cortex subregions support the flexible use of attribute information based on the behavioral operation required to adapt. Under conditions in which a change in outcomes signals that a behavioral switch should occur, accumulating evidence supports the idea that the prelimbic cortex enables a switch in strategies that allows the flexible use of different attribute information, that is, set-shifting. The orbitofrontal cortex enables behavioral flexibility when conditions require a new choice pattern using the same attribute information, that is, reversal learning. The chapter additionally considers a role for the dorsomedial striatum, which receives input from multiple prefrontal areas, in both set-shifting and reversal learning. Based on examination of the error patterns in these different tests, the prefrontal cortex enables behavioral flexibility by initially inhibiting a previous choice pattern and/or generating a new choice pattern while the dorsomedial striatum facilitates the reliable execution of a new choice pattern. It also describes recent findings indicating that the prelimbic cortex along with the subthalamic nucleus and dorsomedial striatum acts in a cooperative manner to enable behavioral flexibility when cues, as opposed to outcomes, guide a proactive behavioral switch. Specifically, the prelimbic cortex and subthalamic nucleus enable the rapid inhibition of an ongoing choice pattern while concomitantly a neural system that includes the prelimbic cortex and dorsomedial striatum enables selection of an alternative choice pattern and maintenance of that selection. Taken together, the Kesner neurobiological model of memory has served as a framework to build substantial support for the idea that prefrontal cortex and basal ganglia structures are crucial to allow rapid and repeated adaptations under changing environmental demands.