Allocentric and egocentric spatial information processing in the hippocampal formation of the behaving primate

Abstract

To investigate how space is represented in the primate hippocampus, the activity of single neurons was recorded in the hippocampus of behaving macaque monkeys. Neurons that responded differently according to the position on a screen in which a stimulus was shown when the monkey had to remember the stimulus and its position were analyzed for their spatial fields. By moving the monkey into different positions relative to the screen, and the screen to different positions in the room, it was possible to separate neuronal representations in egocentric coordinates (i.e., defined relative to the monkey’s body axis) from representations in local allocentric coordinates (i.e., defined relative to the frame of reference provided by the screen on which the stimuli were displayed) and from representations in absolute allocentric coordinates (i.e., defined relative to absolute position in the room). It was found that 44% of the spatial neurons analyzed in these experiments responded in relation to space defined by the local frame of reference and not in relation to space defined in egocentric or in absolute allocentric coordinates. Two percent of the neurons responded in relation to the absolute position of a stimulus in the room (in absolute allocentric coordinates). Ten percent responded in relation to egocentric coordinates. Forty-four percent responded to a combination of the different coordinate systems investigated, including 23% that were shown to include an absolute allocentric component. Thus the main finding was that in the primate hippocampus many spatial cells (69% of those analyzed) responded in relation to allocentric coordinates, in many cases in relation to a local frame of reference and in some cases in relation to the absolute position of the stimulus in the room. In Experiment 2, the possibility of retinotopic encoding was investigated by presenting test spots of light at different positions relative to a fixation spot, and in different blocks of trials by moving the fixation spot to different positions on the screen. It was found that very few hippocampal cells were responsive in this task, and that for the cells that did respond, the encoding was not retinotopic. These results are consistent with the scarcity of egocentric encoding cells, and the preponderance of allocentric encoding, found in Experiment 1. In Experiment 3, it was found that relatively many hippocampal neurons (17%) responded differently according to the spatial position being fixated on the screen, in a task in which a small fixation spot appeared on each trial in a different position on the screen. This result confirms that hippocampal spatial cells do not encode spatial information using retinotopic coordinates, shows that it is sufficient for many of these hippocampal spatial neurons to respond that the monkey fixate particular positions in space, and is consistent with the finding in Experiment 1 that the preponderant type of encoding used by these hippocampal spatial neurons is allocentric.