Functional Connectivity Between the Red Nucleus and the Hippocampus Supports the Role of Hippocampal Formation in Sensorimotor Integration

Abstract

Experiments were carried out in urethane-anesthetized rats to evaluate the hypothesis that the red nucleus has functional connections with the hippocampal formation. Depth profiles of electrical stimulation in experiment 1 confirmed that stimulation administered to the red nucleus elicited theta field activity in the hippocampal formation with a linear relationship between stimulus intensity and theta frequency. Experiment 2 showed that microinfusion of local anesthetic procaine hydrochloride into the medial septum resulted in a reversible blockade of theta field activity elicited by electrical stimulation of the red nucleus. In experiment 3, the discharge activity of red nucleus cells was recorded during the field conditions of hippocampal synchrony (theta) and hippocampal asynchrony [large amplitude irregular activity (LIA)]. Analysis revealed that 26/46 (56%) of red nucleus cells were theta-related, whereas the remaining 20 (44%) were nonrelated. The majority of theta-related cells were classified as tonic theta-on. A brief increase above the basal discharge rate of tonic theta-on red nucleus cells during LIA predicted the transition from LIA to theta with 400- to 500-ms latency. Furthermore, higher frequency transitional discharges predicted higher theta frequencies, whereas higher discharge rates during theta predicted shifts to higher theta frequencies. The results supported the conclusion that the red nucleus, traditionally associated with motor functions, is functionally connected with the neural circuitry involved in the generation of theta band oscillation and synchrony in the hippocampal formation, in agreement with the predictions of the sensorimotor integration model of hippocampal function.