Effect of hippocampal and neocortical spreading depression on rat shuttle behavior in four different experimental paradigms

Abstract

As shown in previous papers, rat shuttle responses to a buzzer (SBs) depend on the operation of three main factors: a state of drive (D) determined by the presence of footshocks in the experimental situation; the pairing (i.e., fixed temporal relation) of buzzers and shocks (P); the contingency (C) of shocks upon SBs. Four tests were studied in which these factors operate in various combinations: (a) D test: 50 buzzers and 25 shocks at random intervals and in random sequence; (b) DP test (Pavlovian conditioning): 50 buzzers paired (contiguous) to shocks on trials, regardless of whether SBs are performed or not; (c) DC test: 50 buzzers, each followed by a shock at a randomly variable interval unless there is an SB on that trial; (d) DPC test (two-way avoidance): 50 buzzers paired to shocks only on those trials in which there is no SB. The effect of hippocampal and neocortical spreading depression on these tests was studied. Spreading depression was induced by the application of KCl crystals through implanted guide cannulae, and was ascertained by EEG recording. Application of KCl on the hippocampus caused both hippocampal and neocortical spreading depression; whereas when it was applied on the neocortex there was only spreading depression in this structure. The following behavioral responses were measured: SBs, jumping to the buzzer, and intertial shuttling. Neocortical spreading depression had no effect on any of these parameters. Hippocampal spreading depression caused an increase of SBs and of intertrial crossings in all four tests, and a depression of jumping responses in the DP test. The increase of SBs was more marked in the D and DC tests. In fact, in the animals with hippocampal spreading depression differences in SB performance between DP and D, or between DPC and DC, were very small and not significant; this was not the case in any of the other groups. Since, as shown previously both DP - D and DPC - DC are a measure of the P factor, these data suggest that the hippocampus normally exerts a tonic inhibitory influence on the operation of D, and that at the same time it plays a role in the operation of P. The results are consistent both with hypotheses which attribute to the hippocampusa role in behavioral inhibition, and with those which consider that it processes stimulus-stimulus dependent information.