Visual properties of human retinal ganglion cells

Abstract

25The retinal output is the sole source of visual information for the brain. Studies in non-primate 26 mammals estimate that this information is carried by several dozens of retinal ganglion cell 27 types, each informing the brain about different aspects of a visual scene. Even though 28 morphological studies of primate retina suggest a similar diversity of ganglion cell types, 29 research has focused on the function of only a few cell types. In human retina, recordings 30 from individual cells are anecdotal. Here, we present the first systematic ex-vivo recording of 31 light responses from 342 ganglion cells in human retinas obtained from donors. We find a 32 great variety in the human retinal output in terms of preferences for positive or negative 33 contrast, spatio-temporal frequency encoding, contrast sensitivity, and speed tuning. Some 34 human ganglion cells showed similar response behavior as known cell types in other primates, 35 while we also recorded light responses that have not been described previously. This first 36 extensive description of the human retinal output should facilitate interpretation of primate 37 data and comparison to other mammalian species, and it lays the basis for the use of ex-vivo 38 human retina for in-vitro analysis of novel treatment approaches. 40Vision starts in the retina, a highly structured part of the central nervous system. The retina 41 performs important signal processing: the incoming images are captured by the 42 photoreceptors, analyzed and split into parallel information streams by retinal circuits, and 43 sent along the optic nerve to higher visual brain centers. Each of the parallel information 44 streams is embodied by a type of ganglion cell and informs the brain about a particular aspect 45 of the visual scene 1 . The non-primate mammalian retina contains over 40 of these different 46 information streams, which can be distinguished based on both functional and morphological 47 criteria 2-7 . 48One striking feature of retinal architecture is that each ganglion cell type tiles the retina so 49 that each feature can be extracted at each location in the visual field. Nevertheless, regional 50 specializations do exist, for example the fovea of the primate retina, a region of very high 51 visual acuity. The foveal region consists almost exclusively of four retinal ganglion cell types, 52 the ON and OFF parasol cells and the ON and OFF midget cells 8-10 , which account for 50-53 70% of all ganglion cells in the primate retina 11 . Functional studies using non-human 54 primates have often focused on these four most abundant retinal ganglion cell types 12-17 . 55 Morphological studies of the complete primate retina, on the other hand, describe a similar 56 variety in ganglion cell types as found in the non-primate retina with at least 17 57 morphologically identified types 11,18-21 . However, functional studies of these non-foveal 58 ganglion cell types in non-human primates have been limited to a set of 7 types 14,22-27 , and 59 physiological assessment of t...

Functional Organization of Midget and Parasol Ganglion Cells in the Human Retina

“…This study concluded that the human retina has a substantially greater diversity of functional cell types than macaque retina, and identified only ~5% of recorded cells that resembled parasol and midget cells, in striking contrast to the numerical dominance of midget and parasol cells in the present results and those of the other recent studies of human retina [12,13], as well as anatomical findings [8,28]. The unique conclusions of this recent study [14] may arise from technical factors. Cell type identification was not confirmed by quantitative clustering (Fig.…”

“…The third recent study [14] described responses of human RGCs to full-field stimuli with temporal frequency sweeps, full-field contrast steps, modulating gratings, and moving bars. A wide range of responses to these stimuli was observed, but quantitative cell type classification was not performed.…”

“…A more detailed study [13] revealed the spatial and temporal properties of four numerically dominant human RGC types that likely correspond to well-studied cell types in macaque --ONparasol, OFF-parasol, ON-midget and OFF-midget --but also suggested a striking differences in temporal visual processing by ON-parasol cells, and only partially characterized their spatial properties and functional organization. A third study [14] probed responses to several kinds of stimuli and proposed a greater diversity of RGC types in human retina than macaque, emphasized by a very low reported proportion of the four major types. These apparently conflicting findings suggest the need for a fuller physiological study of the major RGC types in humans, including their spatiotemporal light response properties and functional organization, in a way that can be directly compared to a large body of work in macaque retina.…”

Electric Stimulation Elicits Heterogeneous Responses in ON but Not OFF Retinal Ganglion Cells to Transmit Rich Neural Information

“…The retina is designed to maximize total retinal information for the least cost [47]. To reveal the mechanism underlying the superb computational efficiency, much work has been devoted to understanding retinal neural codes [25,28,29,34,48,49]. Among several features, the heterogeneity of RGC spiking activities seems central for efficient coding [32][33][34][35][36][37], which better discerns different signals [28,29,34] and reduces the minimal number of cells to convey information [50,51].…”

A novel approach to the functional classification of retinal ganglion cells

“…This code is transmitted to postsynaptic targets in the brain, leading to visual perception. At present, more than 30 RGC types have been identified in the mouse retina [6], and between 15-20 types in the primate and human retina [7,8]. RGC classification is typically based on common anatomical features [9,10], responses to light [6,[11][12][13] or on shared gene expression [4,14,15].…”