Basal ganglia–hippocampal interactions support the role of the hippocampal formation in sensorimotor integration

Abstract

Experiments were carried out to evaluate whether neural activity in the basal ganglia is functionally related to the neural activity underlying mechanisms of theta band oscillation and synchrony in the hippocampal formation. Experiment 1 demonstrated that electrical stimulation administered to the substantia nigra, globus pallidus (GP) and caudate-putamen (CPu) in urethane anesthetized rats elicited theta field activity in the hippocampal formation. Subsequent microinfusion of the local anesthetic procaine hydrochloride into the medial septum reversibly abolished this effect. In Experiment 2, single cell discharge profiles established for 152 cells recorded in nuclei of the basal ganglia resulted in 101 (66%) being classified as theta-related and 51 (34%) classified as nonrelated. Theta-related cells were further subclassified as tonic theta-ON cells ( n = 79) and tonic theta-OFF ( n = 22). Tonic theta-ON and tonic theta-OFF cells displayed irregular or regular (tonic) discharge patterns. Rhythmic discharge patterns did not occur in any theta-related cells in the nuclei of the basal ganglia. However, analyses using Kaneoke and Vitek's [J. Neurosci. Methods 68, (1996) 211] algorithms revealed that 51/101 (50%) theta-related cells displayed periodicity in their discharge patterns whereas 27/51 (53%) of the nonrelated cells displayed periodicity in their discharge patterns. The periodicities in the majority of cells were in frequency ranges above that of theta band oscillation and synchrony. The results support the following conclusions: (1) the cellular activity of the basal ganglia, composed of nuclei 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; (2) the observed functional connectivity provides support for the role of the hippocampal formation in sensorimotor integration.