Regulation of Burst Activity through Presynaptic and Postsynaptic GABA sub(B) Receptors in Mouse Superior Colliculus

In slice preparations, electrical stimulation of the superficial gray layer (SGS) of the superior colliculus (SC) induces EPSC bursts in neurons in the intermediate gray layer (SGI) when GABA sub(A) receptor (GABA sub(A)R)-mediated inhibition is reduced. This preparation has been used as a model system to study signal processing involved in execution of short-latency orienting responses to visual stimuli such as saccadic eye movements. In the present study, we investigated the role of GABA sub(B) receptors (GABA sub(B)Rs) in modulating signal transmission in the above pathway with whole-cell patch-clamp recordings in SC slices obtained from GAD67-GFP knock-in mice. Perfusion of the slice with the GABA sub(B)R antagonist CGP52432 (CGP) greatly prolonged the duration of the EPSC bursts. Local application of CGP to the SGS but not to the SGI produced similar effects. Because SGS stimulation elicited bursts in GABAergic neurons in the SGS when GABA sub(A)Rs were blocked, these results suggest that GABA released after bursts activates GABA sub(B)Rs in the SGS, leading to reduced burst duration. We found both postsynaptic and presynaptic actions of GABA sub(B)Rs in the SGS; activation of postsynaptic GABA sub(B)Rs induced outward currents in narrow-field vertical cells, whereas it caused shunting inhibition in distal dendrites in wide-field vertical cells. On the other hand, activation of presynaptic GABA sub(B)Rs suppressed excitatory synaptic transmissions to non-GABAergic neurons in the SGS. These results indicate that synaptically released GABA can activate both presynaptic and postsynaptic GABA sub(B)Rs in the SGS and limit the duration of burst responses in the SC local circuit.