Intracellular recordings have been made from cat retinal horizontal cells stimulated with flickering test spots. Dim backgrounds increase flicker amplitudes in response to small but not large test stimuli. This background-induced flicker enhancement has been measured for different slit- and square-test stimulus widths and the results compared with two spatial models for the enhancement effect. In the 'dark test-region' model it is argued that rods within the test region are unresponsive to background stimuli because of prior saturation by the test stimulus. Background-evoked rod signals decay passively from regions outside the test stimulus through a syncytial network into the recording site, where they act on the cone-to-horizontal-cell synapse, increasing its gain. In the 'changing length-constant' model rod signals reduce the length constant of a syncytial network by uncoupling the cells within it. This causes an increased response to small but not large test stimuli. Both models are analytically evaluated with the use of a conductive-sheet approximation to the syncytial network. Expressions are derived for network polarization [(V(0, 0)] as a function of stimulus size. The specific stimulus shapes considered are disks, rectangles, slits, and squares in both bright and dark varieties. From these expressions predictions of response enhancement as a function of stimulus size are made for both models. The dark test-region model provides for an exponential decay of flicker enhancement as a function of slit width but a steeper-than-exponential decay with the width of squares, in close agreement with experimental data. The changing length-constant model makes qualitatively similar predictions. Flicker enhancement declines nearly exponentially with slit width. For square-shaped test stimuli the predicted decline of flicker enhancement with size is somewhat shallower than either the dark test-region-model curve or the experimentally determined curve. As recorded in the same set of cells and under the same set of stimulus conditions (with the use of both slit- and square-test stimuli), the mean length constant of the peak-to-peak flicker component in the horizontal-cell response is 168 ± 18 (SE) μm with the background and 232 ± 45 μm in the dark. The mean length constant for the background-induced flicker enhancement, as fit by dark test-region-model curves, is 186 ± 22 μm (n = 9). Thus it seems likely that it is either the horizontal-cell network itself, or a network with a coincidentally similar length constant, that provides the conduit for background-evoked rod signals to enter the test region and induce the flicker-enhancement effect. In amphibia electrical models of horizontal cells suggest that rod backgrounds enhance cone signals by reducing the dark shunt conductance of the rod-to-horizontal-cell synapse. Because in cat the horizontal-cell length constant actually declines slightly during rod-background stimulation, response enhancement is probably not related to this or other conductance-decreasing mechanisms, which would tend rather to increase the length constant. In addition to increasing the peak-to-peak amplitudes of horizontal-cell flicker responses, backgrounds induce a 3- to 5-ms phase advance in flicker waveforms. The advance is greater with small test stimuli than with large test stimuli. Furthermore, regardless of whether the background is present or not, large test stimuli evoke flicker responses that are phase advanced with respect to small stimuli. It is argued that these background- and size-induced phase advances result from the same outer-plexiform-layer mechanism. A feedback model, which incorporates both classic horizontal-cell surround antagonism of cones and enhancement of postsynaptic cone flicker signals, is illustrated. In the model calcium stimulates transmitter release from cones onto horizontal cells, while in turn horizontal-cell membrane potential regulates calcium entry into the cone pedicle.
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