Hippocampal spatial view neurons in primates provide allocentric representations of a view of space 'out there'. The responses depend on where the monkey is looking; and can be updated by idiothetic (self-motion) inputs provided by eye movements when the view is hidden. In a room-based object-place memory task, some hippocampal neurons respond to the objects shown, some to the places viewed, and some to combinations of the places viewed and the objects present in those locations. In an object-place recall task when the location in space at which an object has been seen is recalled by the presentation of the object, some primate hippocampal neurons maintain their responding to the object recall cue in a delay period without the object visible while the place is being recalled; and other neurons respond to the place being recalled. Other spatial view neurons form associations with the rewards present at particular locations in space. These findings, and computational models of the hippocampus, help to show how the primate including human hippocampus is involved in episodic memory.
A fundamental question about the function of the primate including human hippocampus is whether object as well as allocentric spatial information is represented. Recordings were made from single hippocampal formation neurons while macaques performed an object-place memory task that required the monkeys to learn associations between objects and where they were shown in a room. Some neurons (10%) responded differently to different objects independently of location; other neurons (13%) responded to the spatial view independently of which object was present at the location; and some neurons (12%) responded to a combination of a particular object and the place where it was shown in the room. These results show that there are separate as well as combined representations of objects and their locations in space in the primate hippocampus. This is a property required in an episodic memory system, for which associations between objects and the places where they are seen are prototypical. The results thus provide an important advance by showing that a requirement for a human episodic memory system, separate and combined neuronal representations of objects and where they are seen "out there" in the environment, is present in the primate hippocampus.
The primate anterior hippocampus (which corresponds to the rodent ventral hippocampus) receives inputs from brain regions involved in reward processing, such as the amygdala and orbitofrontal cortex. To investigate how this affective input may be incorporated into primate hippocampal function, we recorded neuronal activity while rhesus macaques performed a reward-place association task in which each spatial scene shown on a video monitor had one location that, if touched, yielded a preferred fruit juice reward and a second location that yielded a less-preferred juice reward. Each scene had different locations for the different rewards. Of 312 neurons analyzed in the hippocampus, 18% responded more to the location of the preferred reward in different scenes, and 5% responded to the location of the less-preferred reward. When the locations of the preferred rewards in the scenes were reversed, 60% of 44 hippocampal neurons tested reversed the location to which they responded, showing that the reward-place associations could be altered by new learning in a few trials. The majority (82%) of these 44 hippocampal neurons tested did not respond to reward associations in a visual discrimination, objectreward association task. Thus, the primate hippocampus contains a representation of the reward associations of places "out there" being viewed. By associating places with the rewards available, the concept that the primate hippocampus is involved in object-place event memory is now extended to remembering goals available at different spatial locations. This is an important type of association memory.
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