Ultrastructural and optogenetic dissection of V1 corticotectal terminal synaptic properties

The superior colliculus (SC) is a major site of sensorimotor integration in which sensory inputs are processed to initiate appropriate motor responses. Projections from the primary visual cortex (V1) to the SC have been shown to exert a substantial influence on visually induced behavior, including “freezing.” However, it is unclear how V1 corticotectal terminals affect SC circuits to mediate these effects. To investigate this, we used anatomical and optogenetic techniques to examine the synaptic properties of V1 corticotectal terminals. Electron microscopy revealed that V1 corticotectal terminals labeled by anterograde transport primarily synapse (93%) on dendrites that do not contain gamma aminobutyric acid (GABA). This preference was confirmed using optogenetic techniques to photoactivate V1 corticotectal terminals in slices of the SC maintained in vitro. In a mouse line in which GABAergic SC interneurons express green fluorescent protein (GFP), few GFP‐labeled cells (11%) responded to activation of corticotectal terminals. In contrast, 67% of non‐GABAergic cells responded to activation of V1 corticotectal terminals. Biocytin‐labeling of recorded neurons revealed that wide‐field vertical (WFV) and non‐WFV cells were activated by V1 corticotectal inputs. However, WFV cells were activated in the most uniform manner; 85% of these cells responded with excitatory postsynaptic potentials (EPSPs) that maintained stable amplitudes when activated with light trains at 1–20 Hz. In contrast, in the majority of non‐WFV cells, the amplitude of evoked EPSPs varied across trials. Our results suggest that V1 corticotectal projections may initiate freezing behavior via uniform activation of the WFV cells, which project to the pulvinar nucleus. Electron microscopy revealed that the majority of corticotectal terminals (purple overlay) contact (arrow) small non‐GABAergic dendrites (green overlay). Excitatory postsynaptic responses (green traces) to optogenetic activation of corticotectal terminals (purple) were recorded in vitro in a variety of cell types; wide field vertical cells (green neuron) displayed the most uniform responses.