Abstract
The superficial layers of the superior colliculus (sSC) receive retinal input and project to thalamic regions, the dorsal lateral geniculate (dLGN) and lateral posterior (LP; or pulvinar) nuclei, that convey visual information to cortex. A critical step toward understanding the functional impact of sSC neurons on these parallel thalamo-cortical pathways is determining whether different classes of sSC neurons, which are known to respond to different features of visual stimuli, innervate overlapping or distinct thalamic targets. Here, we identified a transgenic mouse line that labels sSC neurons that project to dLGN but not LP. We utilized selective expression of fluorophores and channelrhodopsin in this and previously characterized mouse lines to demonstrate that distinct cell types give rise to sSC projections to dLGN and LP. We further show that the glutamatergic sSC cell type that projects to dLGN also provides input to the sSC cell type that projects to LP. These results clarify the cellular origin of parallel sSC-thalamo-cortical pathways and reveal an interaction between these pathways via local connections within the sSC.NEW & NOTEWORTHY The superficial layers of the superior colliculus (sSC) project to two visual thalamic targets: the dorsal lateral geniculate (dLGN) and lateral posterior (LP) nuclei. We show that distinct excitatory sSC cell types give rise to these projections; stellate cells project to dLGN and wide-field (WF) cells project to LP. Moreover, these pathways interact via a connection within the sSC from stellate to WF cells.
Highlights
The superficial layers of the superior colliculus receive input from nearly every retinal ganglion cell and visual cortical area (Ellis et al 2016; Wang and Burkhalter 2013), suggesting an important role in visually guided behavior
A study using antidromic stimulation of superficial layers of the superior colliculus (sSC) neurons yielded roughly similar results: the majority of neurons antidromically activated by lateral posterior (LP) stimulation were WF cells, and most dorsal lateral geniculate (dLGN)-projecting neurons were described as NF, stellate, or marginal cells (Mooney et al 1988)
Cre-expressing cells in Rorb Cre transgenic mice (Harris et al 2014) are dense in the upper sSC layers but not the optic fiber layer, where the somas of most WF cells reside. This led us to believe that the Rorb Cre line might facilitate labeling and manipulation of stellate cells independently of WF cells
Summary
The superficial layers of the superior colliculus (sSC) receive input from nearly every retinal ganglion cell and visual cortical area (Ellis et al 2016; Wang and Burkhalter 2013), suggesting an important role in visually guided behavior. The sSC projects to multiple downstream areas including the dorsal lateral geniculate (dLGN) and lateral posterior (LP; or pulvinar) thalamic nuclei. These regions project to and receive input from primary visual cortex (V1) and, in the case of LP, higher order visual cortical areas (May 2006; Oh et al 2014; Roth et al 2016; Zhou et al 2018). These connections likely endow the sSC with important roles in shaping the propagation of visual information to and between visual cortical areas. A study using antidromic stimulation of sSC neurons yielded roughly similar results: the majority of neurons antidromically activated by LP stimulation were WF cells ( some were identified as NF or stellate cells), and most dLGN-projecting neurons were described as NF, stellate, or marginal cells (Mooney et al 1988)
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