Physiological evidence for a trans-basal ganglia pathway linking extrastriate visual cortex and the superior...

Visually responsive regions along the cat's lateral suprasylvian (LS) sulcus provide excitatory inputs to the deep layers of the superior colliculus (SC). It is via this direct cortico-collicular route that LS cortex is thought to enhance the visual activity of SC output neurons and thereby facilitate SC-mediated orientation behaviours. However, it has long been suggested that LS also might influence the SC via an 'indirect' route through the basal ganglia. Such a multi-synaptic route would ultimately modulate SC activity via basal ganglia output neurons in substantia nigra, pars reticulata. Using cortical electrical stimulation, the present experiments in the anaesthetized cat provide a physiological confirmation of this indirect route. Moreover, the patterns of activity evoked in antidromically identified nigro-collicular neurons indicate the involvement of multiple trans-basal ganglia pathways. The most complex evoked patterns consisted of a variable period of inhibition preceded and followed by periods of excitation. Although many neurons displayed only components of this triphasic response, these electrically evoked responses generally matched the characteristics of their responses to natural visual stimuli. Cortical stimulation evoked excitation in all of crossed nigro-collicular neurons and inhibition in the majority of uncrossed nigro-collicular neurons. These data suggest that LS activity accesses multiple trans-basal ganglia circuits that shape nigro-collicular responses that are appropriate for their SC targets. In this way, visual stimuli in one hemifield can be selected as targets for SC-mediated orientation, while simultaneously inhibiting activity in the opposite SC that might generate responses to competing targets.