Proactive behavioral effects of theta-blocking septal stimulation in the rat

The induction of hippocampal theta rhythm using low-frequency septal stimulation has been shown to proactively (1) facilitate the acquisition and (2) increase resistance to extinction of a food-rewarded fixed-ratio (FR) bar-press response (Holt & Gray, Quarterly Journal of Experimental Psychology, 35B, 97-118, 1983). Both (1) and (2) are also seen after septal lesions. This suggests that Holt and Gray's (1983) results may have been due either to stimulation-produced theta waves (the "theta" hypothesis), or a small septal lesion produced by the stimulating current (the "lesion" hypothesis). Both hypotheses were tested in the present experiment using high-frequency septal stimulation. In one of two treatment conditions male Sprague-Dawley rats, chronically implanted with a bilateral septal stimulating electrode and a unilateral bipolar hippocampal recording electrode, received (1) trains of continuous pulses at 77 Hz which blocked the hippocampal theta rhythm, or (2) trains of pulses at 100 Hz interrupted by a 30-msec interval at a frequency of 7.7 Hz. Control animals were implanted but not stimulated. Acquisition of a discrete-trial bar-press response on a fixed ratio 5 reinforcement schedule immediately followed the treatment phase. After 15 days' acquisition all animals were extinguished over the subsequent 12 days. Results indicated that both types of septal stimulation reduced resistance to extinction of barpressing; theta-blocking stimulation produced the greater effect. Theta-blocking stimulation retarded the acquisition of bar-pressing in the early stages of training. These overall results are exactly opposite to those produced by low-frequency (7.7 Hz) theta-driving septal stimulation (Holt & Gray, 1983) and contrary to the predictions of the lesion hypothesis. Furthermore, these findings support the idea that long-term changes in behavior may depend on stimulation-produced changes in the hippocampal theta rhythm.