Control of recurrent inhibition of the lateral posterior-pulvinar complex by afferents from the deep layers of the superior colliculus of the rabbit.

We investigated the effect of stimulation of the deep layers of the superior colliculus (SC) on the recurrent inhibition of the lateral posterior-pulvinar complex (LP) in anesthetized rabbits. Intracellular recordings from 23 relay cells in LP showed that they responded to SC stimulation with a long-lasting (140.2 +/- 19.6 ms; mean +/- SD) inhibitory postsynaptic potential (IPSP), which sometimes was followed by a rebound burst of spikes. The same SC stimulation evoked a burst of spikes in extracellular recordings from 31 recurrent inhibitory interneurons in the LP-cortical pathway, which were located in the ventral part of the visual sector of the thalamic reticular nucleus. The mean latency of the burst in reticular cells was 1.6 ms shorter than that of the IPSP in LP relay cells, suggesting that the IPSP in LP cells was mediated by these reticular cells. Intracellular recordings from nine reticular cells showed that the burst of spikes evoked by SC stimulation resulted from an excitatory postsynaptic potential that was always followed by a long-lasting (143.3 +/- 24.0 ms) IPSP. Stimulation of the contralateral predorsal bundle, the main output pathway of deep SC neurons, elicited similar responses in LP cells or reticular neurons with latencies longer than those from SC stimulation. The latency difference between the responses to predorsal bundle and SC stimulation is equal to the antidromic conduction time of predorsal bundle fibers, suggesting that the inhibition in LP originates from the activation of predorsal bundle-projecting neurons. The response characteristics of the inhibitory circuit of LP and of the lateral geniculate nucleus to SC stimulation are strikingly similar, implying that a similar circuit is used by predorsal bundle-projecting neurons to control the recurrent inhibition in both lateral geniculate nucleus and LP. Because the predorsal bundle-projecting neurons are believed to be involved in the initiation of saccadic eye movements, we suggest that the inhibitory circuits may play an important role in modulating ascending visual information during saccadic eye movements.