Shared and distinct retinal input to the mouse superior colliculus and dorsal lateral geniculate nucleus

• Published in: Journal of neurophysiology Vol. 116; no. 2; pp. 602 - 610
• Main Authors: Ellis, Erika M, Gauvain, Gregory, Sivyer, Benjamin, Murphy, Gabe J
• Format: Journal Article
• Language: English
• Published: United States American Physiological Society 01.08.2016
• Subjects: Action Potentials - physiology; Animals; Animals, Newborn; Female; Geniculate Bodies - cytology; Green Fluorescent Proteins - genetics; Green Fluorescent Proteins - metabolism; Light; Luminescent Proteins - genetics; Luminescent Proteins - metabolism; Male; Mice; Mice, Inbred C57BL; Mice, Transgenic; Microscopy, Confocal; Patch-Clamp Techniques; Rapid Reports; Retina - cytology; Retinal Ganglion Cells - physiology; Superior Colliculi - cytology; Vesicular Glutamate Transport Protein 2 - genetics; Vesicular Glutamate Transport Protein 2 - metabolism; Visual Pathways - physiology; retina; superior colliculus; retinorecipient; thalamus
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00227.2016

The mammalian retina conveys the vast majority of information about visual stimuli to two brain regions: the dorsal lateral geniculate nucleus (dLGN) and the superior colliculus (SC). The degree to which retinal ganglion cells (RGCs) send similar or distinct information to the two areas remains unclear despite the important constraints that different patterns of RGC input place on downstream visual processing. To resolve this ambiguity, we injected a glycoprotein-deficient rabies virus coding for the expression of a fluorescent protein into the dLGN or SC; rabies virus labeled a smaller fraction of RGCs than lipophilic dyes such as DiI but, crucially, did not label RGC axons of passage. Approximately 80% of the RGCs infected by rabies virus injected into the dLGN were colabeled with DiI injected into the SC, suggesting that many dLGN-projecting RGCs also project to the SC. However, functional characterization of RGCs revealed that the SC receives input from several classes of RGCs that largely avoid the dLGN, in particular RGCs in which 1) sustained changes in light intensity elicit transient changes in firing rate and/or 2) a small range of stimulus sizes or temporal fluctuations in light intensity elicit robust activity. Taken together, our results illustrate several unexpected asymmetries in the information that the mouse retina conveys to two major downstream targets and suggest that differences in the output of dLGN and SC neurons reflect, at least in part, differences in the functional properties of RGCs that innervate the SC but not the dLGN.