Unambiguous representation of overlapping serial events in the rat hippocampal formation.

The hippocampal formation is suggested to be crucial in unambiguous representation of overlapping temporal sequences in episodic memory. We hypothesized that, if this was true, the hippocampal formation neurons would differentially respond to the same elements even in different temporal sequences. The present study was designed to investigate hippocampal formation CA1 neuronal activity of rats during performance of a conditional delayed stimulus-response association task in which three stimuli were conditionally and serially presented with a delay. In the task, the pairs of the second and third stimuli were overlapped across the trials, but separated by the preceding first stimuli. Conditioned tones coming from one of three possible directions were followed, after a short delay, by one of three pairs of reinforcement series. The pairs consisted of air puff (aversive sensory stimuli) and tube protrusion (which allowed licking sucrose behavior) in the following combinations: air puff-tube protrusion, tube protrusion-tube protrusion and tube protrusion-air puff. The pairs were interposed by a 2 s delay. The three conditioned tone directions were associated with these three pairs in a one-to-one correspondence, and its association was conditional to three possible conditioned tone frequencies (300, 530, and 1,200 Hz). The responses of 107 neurons to the air puff and tube protrusion were analyzed by two-way ANOVA (task condition x reinforcement situation). Of 42 air puff-responsive and 64 tube protrusion-responsive neurons, 36 and 53 displayed significant main effects and/or significant interaction, respectively. Furthermore, neural responses during the delay periods were dependent on the task conditions. The results indicated that the majority of the hippocampal formation neurons showed task condition- and/or reinforcement situation-dependent responses, suggesting a crucial role of the hippocampal formation in representation of overlapping serial events in episodic memory.