The Synaptic Circuitry of Tectothalamic Pathways Underlying Motion Processing in the Tree Shrew

The mammalian visual system is organized into parallel processing streams that begin in the retina and extend through subcortical structures to cortex. This dissertation investigates the cellular and synaptic organization of two major subcortical visual targets—the dorsal lateral geniculate nucleus (dLGN) and the superior colliculus (SC)—in the tree shrew (Tupaia belangeri), a highly visual, pre-primate species with well-laminated visual nuclei. Using a combination of immunohistochemistry, tract-tracing, high-resolution light and electron microscopy, and 3D reconstruction, I explored how morphologically and molecularly distinct retinal ganglion cell (RGC) types relay visual information through separate anatomical channels, and how local circuit motifs shape downstream processing. In Chapter 2, I focused on the dLGN and found that relay neurons in koniocellular (K) laminae are structurally smaller and uniquely express calbindin, distinguishing them from magnocellular/parvocellular (M/P) relay cells. RGC terminals targeting K versus M/P laminae exhibit distinct morphologies, consistent with their origins from different RGC types. I also identified tectogeniculate (TG) projections from three SC cell types that preferentially innervate K laminae and form VGluT2-positive terminals resembling retinal drivers. These findings support a model in which K laminae are anatomically and molecularly tuned to relay specialized visual information to cortex via dual retinal and tectal input streams. In Chapter 3, I examined the superficial SC (sSC), revealing that retinal and cortical inputs terminate in distinct sublayers, with retinal afferents favoring dorsal regions and cortical terminals targeting ventral layers. I found that only retinal terminals formed synapses with horizontal cell (HC) dendrites, which create a complex inhibitory circuitry with their presynaptic dendrites that extend throughout the mediolateral extent of the dorsal sSC layers. I identified four distinct HC synaptic motifs that suggest these dendrites contribute to feature selectivity in sSC output neurons, particularly the pulvinar-projecting widefield vertical cells that are involved in motion detection. Together, these studies provide new insights into how the dLGN and SC implement parallel processing strategies through both input-specific channels and local microcircuitry. These findings have broader implications for understanding the role of subcortical pathways in visual behaviors and disorders and further establishes the tree shrew as a valuable model for studying visual circuits.