Local Excitatory Network and NMDA Receptor Activation Generate a Synchronous and Bursting Command from the Superior Colliculus

Abstract

The generation of bursting spike activity in the deeper layers of the superior colliculus (SC) is a critical determinant of decision making in the initiation of orienting behaviors, such as saccades. The bursting activity exhibits a typical threshold effect that may arise from a nonlinear signal amplification process in the deeper layers of the SC. We used whole-cell patch-clamp recordings in rat SC slices to investigate the neuronal mechanism underlying the generation of such bursting activity. We found that (1) neurons in the intermediate gray layer [stratum griseum intermediale (SGI)] produce a prolonged bursting response when released from GABA(A) receptor-mediated inhibition, (2) this GABA(A) inhibition may partially arise from inhibitory interneurons within the SGI that are driven synaptically by glutamatergic excitatory inputs to the SC, (3) the bursting is not the result of the intrinsic membrane properties of individual SC neurons but is instead produced by local circuits within the SGI, (4) the bursting is mediated by activation of NMDA receptors, and (5) the bursting can be synchronous among SGI neurons. These results suggest that activation of a local excitatory network within the deeper layers of the SC and NMDA receptor-dependent synaptic transmission after release from GABA(A) inhibition are fundamental mechanisms that may explain the nonlinear signal amplification process in the deeper layers of the SC.