The impact of a corticotectal impulse on the awake superior colliculus

Corticotectal (CTect) neurons of layer 5 are large and prominent elements of mammalian visual cortex, with thick apical dendrites that ascend to layer 1, "intrinsically bursting" membrane properties, and fast-conducting descending axons that terminate in multiple subcortical domains. These neurons comprise a major output pathway of primary visual cortex, but virtually nothing is known about the synaptic influence of single CTect impulses on the superior colliculus (SC). Here, we examine the distribution of monosynaptic currents generated in the superficial SC by spontaneous impulses of single CTect neurons. We do this by recording the spikes of CTect neurons and the field potentials that they generate through the depths of the SC. Methods of spike-triggered averaging and current source density analysis are then applied to these data. We show, in fully awake rabbits, that single CTect impulses generate potent, fast-rising monosynaptic currents in the SC similar to those generated in sensory cortex by specific thalamic afferents. These currents are focal in depth, precisely retinotopic, and highly dependent on the conduction velocity of the CTect axon. Moreover, we show that CTect synapses, like thalamocortical synapses, suffer a chronic state of depression in awake subjects that is modulated by preceding interspike interval. However, CTect neurons generated few "bursts," and postsynaptic responses in the SC were not significantly influenced by a shift from alert to an inattentive state (indicated by hippocampal EEG). Together, our results suggest that single CTect neurons may resemble thalamocortical neurons in their ability to serve as potent "drivers" of postsynaptic targets.