The effects of dark adaptation on the response properties of ganglion cells have been documented extensively in the cat retina. To pinpoint the different retinal mechanisms that underlie these effects, we studied the response characteristics of cat horizontal (H) cells during prolonged dark adaptation. H-cell responses were recorded intracellularly in the optically intact, in vivo eye. To disentangle rod and cone contributions, sensitivity changes during dark adaptation were tracked with white light and with monochromatic lights that favored either rod or cone excitation. Stable, long-lasting recordings allowed us to measure changes of sensitivity for adaptation periods up to 45 min. Thresholds for white light and 503-nm monochromatic light decreased steadily and in parallel. The maximum increase of sensitivity, after extinguishing a photopic adaptation light, was 1.8 log units only, reached after about 35 min. Sensitivity for 581-nm lights also increased steadily, but at a shallower slope. The steady increase of sensitivity was concomitant with a linear shift in resting membrane potential and with an increase in relative rod contribution to the threshold responses. Even though small-amplitude responses were rod dominated after prolonged dark adaptation, sensitivity to rod signals remained relatively low, compared to sensitivity of cone responses or to the absolute sensitivity of ganglion cells. This suggests that the cone-H-cell pathway plays no role in the dark-adapted cat retina.

We have investigated responses in proximal retina of the cat that contribute to two kinds of electroretinogram (ERG) recordings: (1) the pattern ERG, a light-adapted response and (2) the threshold and near threshold ERG, a dark-adapted response (Sieving et al., 1986a, 1986b; Sieving & Steinberg, 1985). In intraretinal, extracellular recordings, two negative-going responses were identified that are maximal around the inner plexiform layer, and distinct from PII, which is maximal in distal retina: under light-adapted conditions, a spatially tuned response at light onset and light offset, the “M-wave” (previously described in cold-blooded animals by Karwoski & Proenza (1977, 1980)), and under dark-adapted conditions, the scotopic threshold response, or “STR,” a response at light onset. The results under dark-adapted conditions are examined in more detail here.

The STR is a very sensitive response whose threshold is 1.5–2.0 log units below that of the dc-component of PII and therefore well below the threshold of the a-, b-, and c-waves. It saturates about 2.4 log units below rod saturation. The STR contributes a negative-going potential to the dark-adapted ERG that is dominant near threshold; while PII (dc-component and b-wave) contributes a positive-going potential that is dominant at higher intensities (Sieving et al., 1986b). Investigation of the mechanism of the proximal retinal responses that contribute to the ERG supports a K+-Müller cell hypothesis of their origin.

Primate retinal ganglion cells that project to the magnocellular layers of the lateral geniculate nucleus (M) are much more sensitive to luminance contrast than those ganglion cells projecting to the parvocellular layers (P). We now report that increasing contrast modifies the temporal-frequency response of M cells, but not of P cells. With rising contrast, the M cells' responses to sinusoidal stimuli show an increasing attenuation at low temporal frequencies while the P cells' responses scale uniformly. The characteristic features of M-cell dynamics are well described by a model originally developed for the X and Y cells of the cat, where the hypothesized nonlinear feedback mechanism responsible for this behavior has been termed the contrast gain control (Shapley & Victor, 1978, 1981; Victor, 1987, 1988). These data provide further physiological evidence that the M-cell pathway differs from the P-cell pathway with regard to the functional elements in the retina. Furthermore, the similarity in dynamics between primate M cells and cat X and Y retinal ganglion cells suggests the possibility that P cells, being different from either group, are a primate specialization not found in the retinae of lower mammals.

Putative GABAergic mechanisms were studied in perfused cat retina by means of intracellular recording and application of GABA and the GABAA agonists δ-amino valeric acid (dAVA), muscimol, and THIP. In contrast to results reported previously for cold-blooded vertebrates, introduction of 20 mM GABA into the superfusate had no influence upon the response properties of cat retinal horizontal cells (HCs). In common with results reported in cold-blooded vertebrates, introduction of the GABAA agonists dAVA (2–12 mM) and THIP or muscimol (0.2–1 mM) had four consistent reversible influences upon the response properties of cat retinal HCs: (1) they reduced photic-response amplitude, (2) slowed response onset, (3) slowed response offset, and (4) depolarized the dark membrane potential. Both rod and cone signal components were affected. GABAA agonists had similar influences upon both the time course and amplitude of responses recorded from amacrine and ganglion cells. In all cell types examined, the influence upon response kinetics was made particularly apparent with rapidly flickering stimuli. Flicker responses were reduced in amplitude much more than sustained responses. These results suggest that, in addition to other influences, GABAergic action serves to modify the time course of photic responses in both the inner and outer plexiform layer of mammalian retina making responses slower and less phasic.

Previous studies of the varibility of firing of retinal ganglion cells have led to apparently contradictory conclusions. To a first approximation, the variance of rate of maintained discharges of ganglion cells in cat is independent of the mean firing rate. On the other hand, the variability of responses to abrupt changes in lighting of ganglion cells in goldfish increascs with increasing firing rate. To examine whether the difference is due to differences between species, we examined the variablility of responses of cat ganglion cells, and find it similar to that of goldfish ganglion cells. The variance of rate of ganglion cells is neither independent of mean rate, as might be expected from maintained dischargs, nor directly proportional to the mean rate, as it is for cat cortical cells. Rather, there is a monlinear relationship between varience of rate and mean rate.

Putative GABAergic mechanisms were studied in the cat retina by exogenous application of the GABAA antagonists picrotoxin (PTX), native bicuculline (BCC), and bicuculline methyl bromide (BCC MeBr). When recording intracellular responses from horizontal cells (HCs) and amacrine cells as well as electroretinograms (ERGs), drugs were added to the perfusate used to maintain the isolated eyecup; when recording extracellular spikes from ganglion cells of anesthetized cats, drugs were introduced by iontophoretic injection. Both PTX and BCC MeBr had relatively little influence upon the response properties of HCs. In contrast, native BCC tended to decrease the amplitude of and to slow the photic response to light onset and both to quicken and to increase the amplitude of response to light offset; in the presence of native BCC, HC responses were dominated by a prominent spike-like “Off-overshoot.” The influence of GABAA agonists upon HC responses was not blocked by GABAA antagonists. ERG b−wave amplitude was reduced both by PTX and by native BCC, but was not influenced by BCC MeBr. Latency (time to half-peak) was increased by low doses of native BCC, and to a lesser extent PTX but not BCC MeBr. Rod-amacrine On-transient responses were increased in amplitude by PTX. Extracellular recordings from On- and Off- X and Y ganglion cell types became considerably more transient with application of either PTX, native BCC, or BCC MeBr; this tendency was greater in Off-type ganglion cells. Collectively, these results strengthen conclusions from the previous paper suggesting that GABA serves to slow onset and offset kinetics of retinal neurons, making them more sustained and less phasic. They also suggest that in mammalian retina heterogeneous types of GABAA receptors exist, segregated into different zones: a distal zone, sensitive only to native BCC, a central zone sensitive to both native BCC and PTX, and a proximal zone sensitive to native BCC, BCC methyl halides (BCC MeH), and PTX. Only the proximal zone obeys conventional GABAA pharmacology.