Relationships between the prefrontal cortex and the basal ganglia in the rat: Physiology of the cortico-nigral circuits

The prelimbic/medial orbital areas (PL/MO) of the rat prefrontal cortex are connected to substantia nigra pars reticulata (SNR) through three main cir cuits: a direct nucleus accumbens (NAcc)-SNR pathway, an indirect NAcc-SNR pathway involving the ventral pallidum (VP) and the subthalamic nucleus (ST N), and a disynaptic cortico-STN-SNR pathway. The present study was underta ken to characterize the effect of PL/MO stimulation on SNR cells and to det ermine the contribution of these different pathways. The major pattern of r esponses observed in the SNR was an inhibition preceded by an early excitat ion and followed or not by a late excitation. The inhibition resulted from the activation of the direct NAcc-SNR pathway because it disappeared after acute blockade of the glutamatergic corticostriatal transmission by CNQX ap plication into the NAcc, The late excitation resulted from the activation o f the indirect NAcc-VP-STN-SNR pathway via a disinhibition of the STN becau se it disappeared after either CNQX application into the NAcc or blockade o f the GABAergic striato-pallidal transmission by bicuculline application in to the VP. The early excitation, which was markedly decreased after blockad e of the cortico-STN transmission by CNQX application into the STN, resulte d from the activation of the disynaptic cortico-STN-SNR pathway. Finally, t he blockade of the cortico-STN-VP circuit by CNQX application into STN or V P modified the influence of the transstriatal circuits on SNR cells. This s tudy suggests that, in the prefrontal cortex-basal ganglia circuits. the tr ans-subthalamic pathways, by their excitatory effects, participate in the s haping of the inhibitory influence of the direct striato-nigral pathway on SNR neurons.