Activity of pallidal and striatal tonically active neurons is correlated in MPTP-treated monkeys but not in normal monkeys

The goal of this study is to assess the function of tonically active neurons (TANs) of the striatum and their malfunction in the parkinsonian state. We recorded multiple spike trains of striatal TANs and pallidal neurons, which are the main target of striatal projections. Recordings were performed in two vervet monkeys before and after the induction of tremulous parkinsonism by systemic injection of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine hydrochloride (MPTP). We then calculated cross-correlograms between TANs and pallidal neurons to evaluate the interactions between them. In the normal monkeys, only 1.3% (2/152) of the cross-correlograms displayed significant peaks, and 8.6% (13/152) displayed significant oscillations. After MPTP treatment, 42.8% (83/194) of the cross-correlograms displayed significant peaks or troughs, or both, and 58.8% (114/194) displayed significant 3-19 Hz periodic oscillations. The frequency content of the coherent oscillations matched the frequency content of the activity of individual TANs, but was only weakly related to that of individual pallidal cells. These results confirm the notion that in the normal state neurons in the basal ganglia tend to fire independently, whereas in the parkinsonian state they exhibit synchronized oscillatory activity. The low level of correlated activity in the normal state demonstrates that TANs have only a slight effect on pallidal activity during execution of familiar behavior. The high level of oscillatory correlated activity in the parkinsonian state further suggests that coherent oscillations of the whole basal ganglia circuitry underlie the clinical features of Parkinson's disease.