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

Erika M Ellis,Gregory Gauvain,Benjamin Sivyer,Gabe J Murphy

doi:10.1152/jn.00227.2016

Abstract

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.

Highlights

Our results suggest that the mouse superior colliculus (SC) has access to input from most of the retinal ganglion cells (RGCs) that innervate the dorsal lateral geniculate nucleus
To estimate the fraction of RGCs that project to a given retinorecipient area requires one to first identify RGCs. This is nontrivial because the ganglion cell layer of the mammalian retina contains both RGCs and a substantial number of amacrine cells, i.e., GABA, and/or glycinergic interneurons that do not project to the brain
To label RGCs selectively, we crossed transgenic mouse lines in which Cre recombinase is expressed in vesicular glutamate transporter 2 (vGlut2)-expressing cells (Vong et al 2011), and the red fluorescent protein TdTomato is expressed in cells that express Cre recombinase (Ai14; Madisen et al 2010)

Summary

Introduction

Our results suggest that the mouse superior colliculus (SC) has access to input from most of the retinal ganglion cells (RGCs) that innervate the dorsal lateral geniculate nucleus (dLGN). One hypothesis is that dLGN and SC neurons exhibit distinct outputs despite receiving input from similar sets of retinal ganglion cells (RGCs); distinct local processing of shared retinal input might be necessary because most (of the small number of) reconstructed rodent and cat RGC axonal arbors innervate both the dLGN and SC (Bowling and Michael 1980; Dhande et al 2011). An alternative hypothesis is that differences in the output of dLGN and SC neurons reflect differences in the retinal input the neurons receive (de Monasterio 1978; Rodieck and Watanabe 1993; Schiller and Malpelli 1977) This is plausible because substantially more RGCs innervate one retinorecipient target than the other (Dreher et al 1985; Linden and Perry 1983; Martin 1986; Perry et al 1984). We satisfied these requirements by determining the fraction of mouse RGCs labeled via injection of rabies virus and/or retrogradely trans-

Methods

Results

Conclusion