Functional Organization of Ganglion Cells in the Salamander Retina

Abstract

Segev, Ronen, Jason Puchalla, and Michael J. Berry II. Functional organization of ganglion cells in the salamander retina. J Neurophysiol 95: 2277-2292, 2006. First published November 23, 2005 doi:10.1152/jn.00928.2005. Recently, we reported a novel technique for recording all of the ganglion cells in a retinal patch and showed that their receptive fields cover visual space roughly 60 times over in the tiger salamander. Here, we carry this analysis further and divide the population of ganglion cells into functional classes using quantitative clustering algorithms that combine several response characteristics. Using only the receptive field to classify ganglion cells revealed six cell types, in agreement with anatomical studies. Adding other response measures served to blur the distinctions between these cell types rather than resolve further classes. Only the biphasic OFF type had receptive fields that tiled the retina. Even when we attempted to split these classes more finely, ganglion cells with almost identical functional properties were found to have strongly overlapping spatial receptive fields. A territorial spatial organization, where ganglion cell receptive fields tend to avoid those of other cells of the same type, was only found for the biphasic OFF cell. We further studied the functional segregation of the ganglion cell population by computing the amount of visual information shared between pairs of cells under natural movie stimulation. This analysis revealed an extensive mixing of visual information among cells of different functional type. Together, our results indicate that the salamander retina uses a population code in which every point in visual space is represented by multiple neurons with subtly different visual sensitivities. I N T R O D U C T I O NIn now classic work, Wässle and colleagues showed that the alpha ganglion cell in the cat, which is distinguished by its large soma size, formed two plexuses with their dendritic arbors-one with ON-type light responses and the other with OFF-type-that precisely covered visual space (Wässle and Boycott 1991). The somas of neighboring cells tended to be spaced one dendritic diameter apart from one another, the tips of their dendrites just barely touching. A similar territorial organization and dendritic coverage factors close to one have been found in other, prominent morphological types of ganglion cells both in the monkey and the rabbit (Dacey 1993;Vaney 1994). Tight correspondences between anatomy and function have also been found (Wässle and Boycott 1991), along with an increasingly intricate functional segregation of axons and dendrites in the inner plexiform layer (MacNeil et al. 1999;Pang et al. 2002;Roska and Werblin 2001;Sterling 1983;Wassle 2004;Zhang et al. 2004). For all these reasons, tiling has come to be regarded as a fundamental principle of retinal organization.However, this simple picture of efficient tiling does not hold for all of the ganglion cells. Several other anatomical types have coverage factors greater than two (Rodieck ...

Genetic Control of Circuit Function:Vsx1andIrx5Transcription Factors Regulate Contrast Adaptation in the Mouse Retina

“…At the temporal maximum of the STA, a general two-dimensional Gaussian was fit to the spatial response profile. Similar to recordings from other species using comparable stimulation conditions (Devries and Baylor, 1997;Segev et al, 2006), receptive field surrounds were weak in our recordings, and fitting receptive field profiles with a difference of Gaussians offered no significant improvement and were therefore not included in the present analysis. The radius of the receptive field (r) was defined as follows:…”

“…This was achieved by making vectors representing the respective parameters unit length, before concatenating them and subjecting them to k-means clustering. Inclusion of the autocorrelation function and/or responses to diffuse light steps did not change our classification (Segev et al, 2006). Instead, it revealed that responses of fast ON cells were more sustained than for medium ON cells, and responses of biphasic OFF cells were more sustained compared with those of monophasic OFF cells (data not shown).…”

“…STAs were calculated from reverse correlation of the spike train to checkerboard stimulation. Cells were clustered into distinct types using agglomerative k-means algorithms on the temporal structure of the STAs (Segev et al, 2006). Approximately 80% of all cells recorded (137 of 169 cells; n ϭ 10 retinas) belonged to one of four functional types identified in this way.…”

Disinhibitory gating of retinal output by transmission from an amacrine cell

“…The responses of different cells are precisely timed in the retina, with different amacrine and ganglion cells having distinct temporal responses with respect to light (6)(7)(8)(9). Inhibitory transmission to ganglion cells is known to have different effects, including reducing activity (6,10), or increasing activity through disinhibition (11)(12)(13)(14).…”

Predictable irregularities in retinal receptive fields

“…S1 for how it is derived. If RFs are described as Gaussians, then the width of the Gaussian is found to be ϷL/2 in different species and types of retinal ganglion cells (2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12) (Fig. 1A), with the exception of some cell types in the salamander retina (5).…”