Parallel processing of information about location in the amygdala, entorhinal cortex and hippocampus

ABSTRACT The conditioned cue preference paradigm was used to study how rats use extra‐maze cues to discriminate between 2 adjacent arms on an 8‐arm radial maze, a situation in which most of the same cues can be seen from both arms but only one arm contains food. Since the food‐restricted rats eat while passively confined on the food‐paired arm no responses are reinforced, so the discrimination is due to Pavlovian stimulus‐reward (or outcome) learning. Consistent with other evidence that rats must move around in an environment to acquire a spatial map, we found that learning the adjacent arms CCP (ACCP) required a minimum amount of active exploration of the maze with no reinforcers present prior to passive pairing of the extra‐maze cues with the food reinforcer, an instance of latent learning. Temporary inactivation of the hippocampus during the pre‐exposure sessions had no effect on ACCP learning, confirming other evidence that the hippocampus is not involved in latent learning. A series of experiments indentified a circuit involving fimbria‐fornix and dorsal entorhinal cortex as the neural basis of latent learning in this situation. In contrast, temporary inactivation of the entorhinal cortex or hippocampus during passive training or during testing blocked ACCP learning and expression, respectively, suggesting that these two structures co‐operate in using spatial information to learn the location of food on the maze during passive pairing and to express this combined information during testing. In parallel with these processes we found that the amygdala processes information leading to an equal tendency to enter both adjacent arms (even though only one was paired with food) suggesting that the stimulus information available to this structure is not sufficiently precise to discriminate between the ambiguous cues visible from the adjacent arms. Expression of the ACCP in normal rats depends on hippocampus‐based learning to avoid the unpaired arm which competes with the amygdala‐based tendency to enter that arm. In contrast, there is cooperation between amygdala‐ and hippocampus‐based tendencies to enter the food‐paired arm. These independent forms of learning contribute to the rat's ability to discriminate among spatial locations using ambiguous extra‐maze cues. © 2013 Wiley Periodicals, Inc.