Monkey hippocampal neuron responses to complex sensory stimulation during object discrimination

The purpose of this study was to investigate, during the performance of an object discrimination task, responses of neurons in the monkey hippocampal formation to the sight of several objects that have biological meaning, and compare these responses with those of amygdalar neurons studies previously using the same task. Neuronal activity in the hippocampal formation of conscious monkeys was recorded during performance of a task that led to presentation of familiar rewarding, familiar aversive, or unfamiliar objects. Of 864 neurons recorded in the hippocampal formation and adjacent cortices, 160 (18.5%) responded to the sight of a certain object(s). Responses to the sight of different kinds of objects were analyzed in detail. Nondifferential neurons (n = 73) responded to different objects with no significant difference in response magnitudes, and differential neurons (n = 87) responded to different objects with different response magnitudes. Of the differential neurons, 23 responded more strongly to rewarding objects than to other objects (rewarding‐object‐dominant neurons), but the magnitude of responses to objects did not necessarily correlate with the order of preference to the objects as determined from observation of animal behavior. Aversive‐object‐dominant neurons (n = 13) responded more to aversive objects than to other objects. Unfamiliar‐object‐dominant neuron (n = 7) responded more to unfamiliar objects than to familiar objects. Selective neurons (n = 10) responded selectively to only one object or one category of objects. Fourteen of the rewarding‐ or aversive‐object‐dominant neurons were tested in extinction or reversal trials. In 12 of 14 neurons, responses to a rewarding or aversive object did not change, or slightly weakened, in extinction or reversal trials. The results suggest the following. (1) Responses of rewarding‐or aversive‐object‐dominant neurons may be involved in object‐reward or object‐aversion association. However, responses of many of these neurons might reflect past inputs related to reinforcement rather than extant emotional processing. (2) Responses of unfamiliar‐object‐dominant neurons may be involved in recognition of objects based on their familiar or unfamiliar aspects. These results are further discussed and compared with responsiveness of amygdalar neurons.