Hippocampal neuronal mechanisms of coordination of two concurrently relevant spatial representations

Abstract

How distinct concurrently relevant neural representations are organized in a neuronal network is an important and controversial theoretical question with potentially significant clinical implications. We recorded the activity of populations of hippocampal CA1 neurons in a two-frame room+arena+ place avoidance task in which a rat was exposed to two different sets of landmarks that were continuously dissociated. The rat was walking on a slowly rotating arena (1 rpm), and its position could be defined in two frames of reference – in the stationary room frame and in the rotating arena frame. The rat was reinforced to avoid two shock zones; one was defined relative to the room, the other relative to the arena. The rats avoided both shock zones; we infer that they processed information about their position in both frames of reference. The rats’ position in both spatial reference frames was reflected in the activity of the hippocampal place cells. Neurons recorded during the same session displayed cohesive responses; they tended to code preferentially for the same frame of reference. The firing of hippocampal place cells was coordinated on the timescale of the theta rhythm. Cells coding for similar representations were activated together while cells coding for distinct representations were active at different times. We also observed switching between two distinct states of hippocampal activity within single experimental sessions of the room+arena+ place avoidance. These data suggest that hippocampal neurons were organized into functionally defined groups and that only one group of functionally related neurons was preferentially active at any given time. This functional organization provided a potential mechanism of coordination of multiple concurrently relevant representations.