Pre-movement activities in neurons in the intermediate gray layer (stratum griseum intermediale, SGI) of the mammalian superior colliculus (SC) are essential for initiation of orienting behaviors such as saccades. Our previous study has demonstrated that burst activities are induced by synchronous activation of SGI neurons communicating within a local excitatory network, which depends on NMDA receptor-dependent synaptic transmission and release from GABA_A inhibition. Furthermore, dual whole-cell recordings from adjacent neurons in SGI have revealed that application of 10 µM bicuculline (Bic) and reduction of extracellular Mg²⁺ concentration (to 0.1 mM) induce spontaneous depolarization that is synchronous between neuron pairs, suggesting the recruitment of a large number of neurons communicating through intense excitatory connections. In the present study, we investigated the properties of synchronous depolarization, and the fundamental structure of the lateral excitatory network that recruits a neuronal population in SC to synchronous activation, by analyzing the synchronicity of spontaneous depolarization induced in the presence of Bic plus low Mg²⁺. We have found that 1) spontaneous depolarization exhibits bidirectional horizontal propagation among the SGI neuron pairs, 2) induction of spontaneous depolarization is not caused by activation of intrinsic voltage-dependent conductances, 3) neurons exposed to low Mg²⁺ alone exhibit spontaneous depolarization, but in this case the depolarization is less synchronous, and 4) neurons exposed to Bic alone exhibit synchronous depolarization, but less frequently than those exposed to both Bic and low Mg²⁺. Analysis of the synchronicity of spontaneous depolarization indicates that the distribution of lateral excitatory connections is markedly different among layers of SC; the SGI neurons form extensive lateral excitatory connections, whereas they are sparse or limited within subsets of neurons in the stratum griseum superficiale (SGS). Wide-field vertical neurons in the stratum opticum have features intermediate between neurons in the SGS and SGI. Such differences in the structure of lateral excitatory connections may reflect the different way signal processing is achieved in each layer of SC.