Responses of ganglion cells to contrast steps in the light-adapted retina of the tiger salamander

Abstract

The impulse discharge of single ganglion cells was recorded extracellularly in superfused eyecup preparations of the tiger salamander (Ambystoma tigrinum). Contrast flashes (500 ms) were applied at the center of the receptive field while the retina was light adapted to a background field of 20 cd/m2. The incidence of cell types in a sample of 387 cells was: ON cells (4%), OFF cells (28%), and ON/OFF cells (68%). Quantitative contrast/response measurements were obtained for 83 cells. On the basis of C50, the contrast necessary to evoke a half-maximal response, ON/OFF cells fell into 3 groups: (1) Positive Dominant (26%), (2) Balanced (23%), and (3) Negative Dominant (51%). Positive Dominant cells tended to be relatively contrast insensitive. On the other hand, many Negative Dominant cells showed remarkably low C50 values and very steep contrast/response curves. Contrast gain to negative contrast averaged 8.5 impulses/s/% contrast, some four times greater than that evoked by positive contrast. In most ON/OFF cells, the latency of the first spike evoked by a negative contrast step was much shorter (40-100 ms) than that evoked by a positive contrast step of equal contrast. OFF cells typically showed higher C50 values, larger dynamic ranges, and longer latencies than those of Negative Dominant ON/OFF cells. Thus, different pathways or mechanism apparently mediate the off responses of OFF and ON/OFF cells. In sum, the light-adapted retina of the tiger salamander is strongly biased in favor of negative contrast, as shown by the remarkably high contrast sensitivity and faster response of Negative Dominant cells, the remarkably low incidence of ON cells, and the insensitivity of Positive Dominant cells. Some possible underlying influences of bipolar and amacrine cells are discussed.

A retinal circuit model accounting for wide-field amacrine cells

“…As illustrated in Fig. 3, off-BC kernels have faster kinetics than the on-BC kernels in accordance with the prior experimental observations (Burkhardt et al 1998). Main result presented in Fig.…”

Retinal Ganglion Cells Can Rapidly Change Polarity from Off to On

“…In the salamander, the predominance of Off-type retinal responses is evident regardless of how one samples the optic nerve signals [42–44]. Even among the On-Off ganglion cells, there is a strong bias toward the Off pathway under baseline conditions [45] (Figure 6A). However, during the brief period that encodes saccade-related changes in the image, this bias transiently disappears, and over the entire population of ganglion cells, the On responses are as frequent as Off responses (Figure 6B).…”

Faster Thalamocortical Processing for Dark than Light Visual Targets

“…Previous in vitro recordings in the retinas from salamanders and turtles found response latencies that were 30 milliseconds longer (salamanders) and up to 10 times longer (turtles) in ON than OFF bipolar cells (Baylor and Fettiplace, 1977; Copenhagen et al, 1983; Shiells and Falk, 1995; Burkhardt et al, 1998; Gollisch and Meister, 2008; Burkhardt, 2010). This temporal difference was explained by the slower kinetics of the ON glutamate receptor (Nakajima et al, 1993) and the longer axons of ON bipolar cells (Euler et al, 1996), among other factors.…”

“…While there is evidence that the OFF pathway is 30 milliseconds faster than the ON pathway in salamanders (Shiells and Falk, 1995; Burkhardt et al, 1998; Gollisch and Meister, 2008; Burkhardt, 2010), there is no evidence for a faster OFF pathway in mammals. In fact, in vitro measurements in the peripheral retina of primates found faster response time-courses in ON than OFF retinal ganglion cells (Chichilnisky and Kalmar, 2002).…”

“…Just based on the receptor kinetics, it has been estimated that ON bipolar cells in salamanders and turtles can be delayed by 30 milliseconds from OFF bipolar cells (Shiells and Falk, 1995; Burkhardt et al, 1998; Gollisch and Meister, 2008; Burkhardt, 2010) (Baylor and Fettiplace, 1977; Copenhagen et al, 1983). Such temporal differences are likely to be smaller in warm-blooded retinas, particularly if some ON bipolar cells have inotropic AMPA receptors in addition to mGluR6 (Vardi et al, 1998).…”