A Role for Synaptic Input Distribution in a Dendritic Computation of Motion Direction in the Retina

Abstract

Summary The starburst amacrine cell in the mouse retina presents an opportunity to examine the precise role of sensory input location on neuronal computations. Using visual receptive field mapping, glutamate uncaging, two-photon Ca2+ imaging, and genetic labeling of putative synapses, we identify a unique arrangement of excitatory inputs and neurotransmitter release sites on starburst amacrine cell dendrites: the excitatory input distribution is skewed away from the release sites. By comparing computational simulations with Ca2+ transients recorded near release sites, we show that this anatomical arrangement of inputs and outputs supports a dendritic mechanism for computing motion direction. Direction selective Ca2+ transients persist in the presence of a GABA-A receptor antagonist, though the directional tuning is reduced. These results indicate a synergistic interaction between dendritic and circuit mechanisms for generating direction selectivity in the starburst amacrine cell.

Orientation Selectivity in the Retina: ON Cell Types and Mechanisms

“…Given the striking abundance of OSGCs in these two mammalian species, as well as reports of OSGCs in primates (Passaglia et al, 2002), it is likely that these cells directly contribute to orientation selectivity in higher visual centers. In line with this idea, several studies in rodents and primates have identified orientationselective neurons in noncortical areas, such as the dorsal lateral geniculate nucleus (dLGN; Cheong et al, 2013;Piscopo et al, 2013) and superior colliculus (Wang et al, 2010). Further supporting this possibility, recent studies have shown that mouse dLGN axonal projections provide orientation-selective inputs to primary visual cortex (Sun et al, 2016) and that inactivating primary visual cortex does not change the orientation tuning of dLGN neurons (Zhao et al, 2013).…”

“…By comparison, our understanding of the mechanisms generating orientation selectivity in the retina is still rudimentary, largely due to the lack of specific molecular markers. Additionally, there is a drive to characterize the diversity of ganglion cell types, or feature channels, based on their functional, morphological, and genetic profiles (Baden et al, 2016). To date, how many OSGC types are present in the retina and how evolutionarily conserved they are across species remains unclear.…”

“…For example, the alignment of dendrites along a preferred direction has a role in generating direction selectivity in some ganglion cells (Kim et al, 2008). To describe the dendritic morphology of ON-OSGCs and assess its potential role in generating orientation tuning, Nath and Schwartz (2016) and Venkataramani and Taylor (2016) filled functionally identified ON-OSGCs with fluorescent dyes.…”

“…If scenario (2) is correct, the difference in their dendritic morphology is coincidental, not causative of orientation selectivity. Experiments mapping presynaptic inputs using 3D electron microscopy tracing (Briggman et al, 2011), high-resolution immunohistochemistry (Sigal et al, 2015), or neurotransmitter sensors/uncaging (Yonehara et al, 2013;Vlasits et al, 2016) would provide evidence on whether orientation selectivity is a consequence of a bias in the distribution of inputs on their dendritic arbors.…”

“…In a previous study, Venkataramani and Taylor (2010) described two types of rabbit cardinal axes-tuned OFF-OSGCs, and in Venkataramani and Taylor (2016) they conclude that, collectively, OSGCs account for ϳ5% of all rabbit ganglion cells. In a comprehensive functional classification of mouse ganglion cells, Baden et al (2016) identified ON, OFF, and ON-OFF OSGCs comprising different cardinally and obliquely tuned types, which collectively represent ϳ15% of the retinal output. Given the striking abundance of OSGCs in these two mammalian species, as well as reports of OSGCs in primates (Passaglia et al, 2002), it is likely that these cells directly contribute to orientation selectivity in higher visual centers.…”