Comparison of spontaneous and septally driven hippocampal theta field and theta-related cellular activity

Experiments were carried out for the purpose of comparing the electrophysiological properties of spontaneously occurring hippocampal theta field activity with those of theta-like field activity elicited by 5-Hz and 7-Hz electrical stimulation of the medial septum in urethane-anesthetized rats. Experiment 1 compared the amplitude and phase depth profiles for the three conditions of spontaneously occurring theta, theta elicited by 5-Hz medial septal stimulation, and theta elicited by 7-Hz medial septal stimulation. The results supported the conclusion that septally elicited theta field activity exhibited characteristics similar to those of spontaneously occurring theta field activity. Experiment 2 compared the discharge properties of hippocampal theta-related cellular discharges during spontaneous and septally elicited theta field activity. In contrast to the results of Experiment 1, the findings of Experiment 2 supported the conclusion that electrical stimulation of medial septal nuclei did not produce typical responses of hippocampal theta-related cellular activity. During spontaneously occurring field conditions, HPC theta-ON cells increased their discharge rates during spontaneous theta field activity, relative to LIA, and theta-OFF cells decreased (often to zero) their discharge rates during theta field activity relative to LIA. During septally elicited theta-like activity, phasic and tonic theta-ON cells decreased their discharge rates (some were totally inhibited), and most tonic theta-OFF cells increased their discharge rates (although two were totally inhibited). In addition, the discharges (albeit reduced) of the majority of both phasic and tonic theta-ON cells during septal driving became entrained to the stimulation pulses and thus exhibited rhythmicity and strong phase relations with the field activity. Furthermore, both cell types discharged near the positive peak of the septally elicited theta field activity during 5-Hz stimulation and near the negative peak during 7-Hz stimulation. The discharges of most tonic theta-OFF cells also became entrained to the stimulation pulses and exhibited similar phase relations to theta-ON cells during the 5-Hz and 7-Hz driving frequencies. Thus, based on cellular evidence, electrical stimulation of the medial septum activates the hippocampal neural circuitry involved in the generation of theta field activity in a nonphysiological manner. The findings of the present paper provide an explanation for why electrical stimulation of the medial septum in freely moving rats elicits a theta-like field activity that is dissociated from the normal behavioral correlates, in contrast to those elicited by stimulation of the posterior nucleus of the hypothalamus (Bland and Oddie. 2001. Behav Brain Res 127:119-136).