Priming pattern determines the correlation between hippocampal theta activity and locomotor stepping elicited by stimulation in anesthetized rats

Abstract

The after-effects of locomotor stimulation are a transient facilitation of locomotor initiation (the priming effect), and a transient increase in hippocampal rhythmic slow activity in the 3–6 Hz band of the theta range. The similar time course of the two effects suggests that hippocampal 3–6 Hz activity may be linked to the excitability of locomotor initiation. This study tested the hypothesis that power in the 3–6 Hz band that is present prior to stimulation would predict the magnitude of elicited stepping. Stimulation electrodes were implanted in 15 locomotor sites of 10 anesthetized rats (urethane, 800 mg/kg). Hindlimb stepping was elicited by a single control train of electrical stimulation presented once every 62 s. On test trials, a test train at the same intensity followed the control train at varying control/test intervals (15–36 s) to assess the priming effect on stepping. The priming pattern determined whether hippocampal 3–6 Hz power predicted the amount of stepping to be elicited by a stimulation train. Positive correlation (0.47> r>0.22) was found for seven out of eight sites showing positive priming effects. Correlation was absent for three other sites that showed non-significant priming effects and were mixed for four sites that showed negative effects. Sites with positive priming patterns, compared to sites with inconsistent or negative priming patterns, had similar trends in post-stimulation 3–6 Hz power, smaller increases in 6–8 Hz power during the control train and lower 1–3 Hz power during the periods immediately before the control stimulation. For six of 15 sites, regardless of the priming pattern, 1–3 Hz power was inversely related to subsequent stepping, and in three cases provided an independent predictor of stepping. Stimulation at two sites produced discrete episodes of post-stimulation stepping. In one of these cases, a 0.5-Hz increase in peak frequency of hippocampal activity preceded stepping. The results show that the association between hippocampal 3–6 Hz activity and the excitability of locomotor initiation is sufficiently specific to allow prediction of the magnitude of stepping by the prior levels of 3–6 Hz power. However, the occurrence of negative priming effects during prominent 3–6 Hz activity indicates that other factors determine the actual stepping and they can suppress the correlation between theta activity and subsequent locomotion.