Behavioral Correlates of Neuronal Activity Recorded as Single-Units: Promises and Pitfalls as Illustrated by the Rodent Head Direction Cell Signal

The purpose of this chapter is to provide an overview of a current approach in defining the relationships between the firing patterns of groups of neurons recorded from the freely behaving rodent. The design and construction of a 16-channel headstage and its typical integration with a commercially available multichannel data acquisition system is described in detail. Next, the chapter examines the strategies necessary to test the behavioral significance of firing patterns of individual neurons recorded from behaving animals. A discussion is included that surveys the limitations and advantages inherent in testing how discrete behavioral events are represented in single-unit activity recorded from rodents engaged in spatial and nonspatial behaviors. To expand on the technological and theoretical approaches to establishing the relationship between single-unit activity and behavior, the rodent head direction cell system is described as one useful model system. The head direction cell is considered by many to represent the directional sense of the organism and to be essential for spatial navigation. The chapter provides a critical overview of the studies that have been conducted to date to test this relationship. In short, these are the record while the rodent performs some navigational task experiments. Examination of the results from the studies reveals that there is little clear evidence to support the view that head direction cells guide spatial navigation. The ensuing discussion addresses putative reasons for the division between the empirical data and the theory of head direction cell – behavior relations. The chapter concludes with clear suggestions for alternative experimental approaches that might better address brain–behavior relationships. A plea for increased open dialogue between the fields of behavioral analysis and systems/cellular neurophysiology emerges. Improved understanding of the contributions to the neuroscience field made by behavioral neuroscientists and those by electrophysiologists should raise the bar of modern approaches to brain–behavioral relationship studies using in vivo electrophysiological methods.