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Recurrent inhibitory circuitry in the deep layers of the rabbit superior colliculus

1 Local inhibition in the deep layers of the superior colliculus plays a crucial role in sensorimotor integration. Using intracellular and extracellular recording techniques, we studied the organization of inhibitory circuits in the deep layers of the superior colliculus in anaesthetized rabbits. 2 We identified a new cell type in the deep superior colliculus that showed a characteristic burst response to stimulation of both the predorsal bundle and optic chiasm. The response had a jittering latency and failed to follow high frequency stimuli, indicating trans‐synaptic (orthodromic) events. Moreover, the predorsal bundle stimulation‐evoked orthodromic response could be made to collide with the response to a preceding stimulation of the optic chiasm, suggesting that burst‐firing cells received excitatory inputs from the axonal collaterals of predorsal bundle‐projecting cells. 3 Stimulation of the predorsal bundle could evoke an IPSP in predorsal bundle‐projecting cells. The latency of the IPSP was 0·5‐1·0 ms longer than the orthodromic response in burst‐firing cells. Simultaneous recordings showed that the IPSP in predorsal bundle‐projecting cells was preceded by a burst of extracellular spikes from burst‐firing cells with short latency (≈0·9 ms), indicating an inhibitory monosynaptic connection from burst‐firing cells to predorsal bundle‐projecting cells. 4 Burst‐firing cells exhibited a prolonged depression after the predorsal bundle or optic chiasm stimulation due to an inhibitory postsynaptic potential. Latency analysis implies that burst‐firing cells may form mutual inhibitory connections. 5 Together our results suggest that burst‐firing cells and predorsal bundle‐projecting cells form reciprocal excitatory and inhibitory connections and burst‐firing cells may function as the recurrent inhibitory interneurons in the deep layers of the rabbit superior colliculus.