Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on...

The striato-nigro-collicular pathway is one of the neuronal circuits through which basal ganglia can influence ocular and cephalic motricity. Through this pathway striatal signals are conveyed to a major collicular efferent system i.e. the tecto-spinal/tecto-diencephalic neurons (TSD). A striking particularity of the striato-nigro-collicular connection is to present an assemblage of two successive GABAergic inhibitory links. To analyze how striatal information is expressed through this double inhibitory system we made use of concomitant unitary recordings of substantia nigra pars reticulata (SNR) and TSD activity while nigral and/or striatal activity was changed by local applications of pharmacological agents. We observed (1) that an intranigral application of GABA which transiently abolishes the tonic discharge of SNR cells, causes the TSD cells to discharge vigorously. During this period of increased excitability the responsiveness of TSD cells to somatosensory input is significantly enhanced; (2) that an intrastriatal injection of glutamate which silences the nigro-collicular cells, causes the TSD cells to discharge. This striatally induced tectal firing being sensitive to intranigral application of a GABA antagonist (bicuculline), led us to the conclusion that striatum exerts a facilitatory influence on TSD cells by releasing these neurons from the tonic inhibitory nigral influence. The functional implication of such a mechanism is discussed in the light of the current knowledge on the involvement of basal ganglia in eye/head orienting movements.