Spatial responsiveness of monkey hippocampal neurons to various visual and auditory stimuli

To investigate involvement of the hippocampal formation in spatial information processing, activity of neurons in the hippocampal formation of the conscious monkey was recorded during presentation of various visual and auditory stimuli from several directions around the monkey. Of 1,047 neurons recorded, 106 (10.1%) responded to some stimuli from one or more directions. Of these 106 neurons with directionally differentiating responsiveness, 49 responded to visual stimulation, 35 to auditory stimulation, and 22 to both. Among 81 neurons, each tested with more than 10 different stimuli, one type responded independent of the nature of the stimulus (nonselective, n = 39), and responses of the other type depended on the nature of the stimulus (selective, n = 42). To investigate effects of change in spatial relations between test stimuli and background stimuli fixed on the monkey or fixed in the environment, 59 of 106 neurons were tested while the experimental apparatus holding the stimulus was moved relative to the monkey. Of these 59 neurons, 36 changed their responsiveness; 7 maintained the magnitude of their responses but changed the response direction with the movement of the apparatus, 5 changed direction regardless of the movement, and 24 did not change direction, but decreased or extinguished responses from the preferred direction. Thirty-two of 106 neurons were also tested by rotating the monkey. The directionally differentiating responsiveness of 11 neurons followed the monkey (egocentric neurons), that of 9 remained in place in the environment (allocentric neurons), and responses of 12 were reversibly extinguished when the monkey was rotated. The results suggest that these hippocampal neurons may be involved in identification of relations among various kinds of stimuli in different spatial frameworks (egocentric or allocentric) and this identification may be developed from multiple sensory modalities.