Individual Pulvinar Neurons Integrate Cortical and Subcortical Signals

The pulvinar nucleus (PUL) has long been proposed as an integrative hub for sensory processing, but whether this integration occurs at the level of individual neurons or through parallel pathways remains an open question. In this study, we focused on regions of the PUL that receive input from widefield vertical (WFV) neurons of the superior colliculus to investigate synaptic properties across PUL subdivisions. Using a variety of anatomical, optogenetic, and in vitro physiological techniques in male and female mice, we show that WFV inputs to the PUL define two subregions: a caudal medial region (Pcm) that receives bilateral nontopographic WFV input and a lateral region (Pl) that receives ipsilateral topographic WFV input. Electron microscopy revealed that terminals arising from WFV neurons are similar in size across both PUL subdivisions; they are significantly larger than terminals originating from cortical Layer 6 (L6) and significantly smaller than terminals originating from cortical L5. On average, optogenetic activation of WFV terminals in the Pcm evoked responses that displayed short-term synaptic facilitation, like responses to photoactivation of L6 inputs, whereas responses in the Pl displayed short-term synaptic depression similar to responses to photoactivation of L5 inputs. Finally, employing dual-opsin optogenetics, we found a high degree of convergence of ipsilateral and contralateral WFV and L5 and L6 input on individual PUL neurons in both the Pcm and Pl. Taken together, our results reveal subregion-specific responses to WFV input and widespread integration of both cortical and subcortical inputs by individual PUL neurons.