Spatial and behavioral correlates of hippocampal neuronal activity.

The firing rate of hippocampal neurons in rats was related both to spatial location and to multiple behavioral variables as rats performed 2 kinds of tasks that rely on hippocampal function: a spatial navigation task similar in performance demands to the radial-arm maze task and a simultaneous cue odor-discrimination task. In the place task, most cells had distinct single or multiple place fields, that is, neurons increased firing when the rat was in a particular location or locations. However, in most of these cells, firing rate also varied systematically in relation to behavioral variables, including the speed, direction, and turning angle of the rat as it moved through the place field. In addition, the activity of most cells was time-locked to task-relevant approach movements. In the odor task, most cells fired as the rat sampled discriminative cues or when it executed specific, task-relevant approach movements. Some cells fired selectively in relation to which odors were presented, the configuration of odor cues, the locus of the response, or a combination of these variables. Many cells with spatial correlates in the place task also had striking behavioral correlates when rats performed the odor task in the same environment, and the locus of the increased firing associated with behavior in the odor task was not the same as the place field in the place task. Thus, while the complex stimuli that compose spatial cues are reflected in hippocampal neuronal activity, hippocampal processing is not limited to the representation of spatial location. Rather, the domain of hippocampal representation includes both spatial and nonspatial relations among multiple cues and the actions directed in relation to these cues, across cue modalities, and across behavioral paradigms.