Horizontal cells reveal cone type-specific adaptation in primate retina

Abstract

The human cone visual system maintains contrast sensitivity over a wide range of ambient illumination, a property known as light adaptation. The first stage in light adaptation is believed to take place at the first neural step in vision, within the long, middle, and short wavelength sensitive cone photoreceptors. To determine the properties of adaptation in primate outer retina, we measured cone signals in second-order interneurons, the horizontal cells, of the macaque monkey. Horizontal cells provide a unique site for studying early adaptational mechanisms; they are but one synapse away from the photoreceptors, and each horizontal cell receives excitatory inputs from many cones. Light adaptation occurred over the entire range of light levels evaluated, a luminance range of 15-1,850 trolands. Adaptation was demonstrated to be independent in each cone type and to be spatially restricted. Thus, in primates, a major source of sensitivity regulation occurs before summation of cone signals in the horizontal cell.

Figure 1

(a) The light stimulus applied to the retina was a temporal waveform (Top) created by adding a high-frequency (19.52-Hz), low-amplitude test wave (Bottom) to a low-frequency (0.61-Hz), high-amplitude vehicle wave (Middle). Mean illuminance was 1,000 tds, and the contrast of the vehicle wave was 0.85. (b) HI horizontal cell response to luminance stimuli (5° field). (Top) Combined-wave response. (Middle) Response to vehicle wave alone. (Bottom) The difference wave obtained by subtraction. The test response varied with vehicle-wave phase. (c) First-harmonic amplitude of each cycle of the difference-wave response shown in b is plotted against vehicle-wave phase at 1,000 tds (○) and 100 tds (●). Solid lines show fit of the data by the inverse sine equation r = A/(BCsin(Φ_M + Φ_lag) + 1), where Φ_M is the vehicle-wave phase and C is vehicle-wave contrast. Free parameters are A, which is an overall scaling parameter, B, which scales the sine wave amplitude and is a measure of the degree of adaptation, and Φ_lag, representing an adaptation delay. (d) Equivalent data for a second H1 cell. At 1,000 tds the mean value of B was 0.77 (n = 32, SD = 0.14) and the mean Φ_lag corresponded to a delay of 41.4 msec (n = 32, SD = 0.14 msec). At 100 tds the mean value of B was 0.46 (n = 16, SD = 0.11) and the mean Φ_lag corresponded to a delay of 59.0 msec (n = 16, SD = 0.33 msec). In separate experiments, test amplitude was found to be linearly related to contrast over the range tested (not shown).

Figure 2

Voltage responses of an HI horizontal cell to cone isolating stimuli (mean illuminance, 1,000 tds; 5° field as in Fig. 1). LED contrasts for cone-isolating conditions are given in Materials and Methods. (a) Same-cone condition: an L-cone-modulating vehicle wave was added to an L-cone-modulating test wave. Difference wave (bottom trace) shows that L-cone modulation affected response amplitude to L-cone test wave. (b) Cross-cone condition: an M-cone-isolating test wave was added to the L-cone-isolating vehicle wave. In this condition amplitude of the response to the M-cone test was not changed by the L-cone vehicle wave (see also Fig. 3a).

Figure 3

HI and HII horizontal cell voltage response amplitudes to cone-isolating test waves plotted as a function of vehicle-wave phase (mean illuminance, 1,000 tds; 5° field). (a and b) Responses of an HI horizontal cell to cone-specific modulation. (a) L-cone vehicle-wave condition: L-cone test response amplitude varied with vehicle-wave phase (●) but M-cone test response did not (○). (b) M-cone vehicle-wave condition: M-cone test response amplitude varied with vehicle-wave phase (●) but L-cone test response did not (○). (c and d) Responses of an HII horizontal cell to cone-specific modulation. (c) S-cone vehicle-wave condition: S-cone test response amplitude varied with vehicle-wave phase (●) but (L+M)-cone test response did not (○). (d) (L+M)-cone vehicle-wave condition: (L+M)-cone test response amplitude varied with vehicle-wave phase (●) but S-cone test response did not (○). Solid lines are fits of equation given in the legend to Fig. 1.

Figure 4

Test for spatial interaction between vehicle and test waves in the HI horizontal cell receptive field. (a) Spatially separate condition: when the test wave (100 td average, 1.00 contrast) was delivered to a central spot and the vehicle wave (900 td average, 0.90 contrast) was delivered to a contiguous, surrounding annulus (see Inset), the vehicle wave did not affect the test-wave response. (b) For the same cell, when vehicle and test waves are spatially superimposed, test response is modulated as in Fig. 1. Vehicle contrast was adjusted to give a similar response amplitude as in a (vehicle wave: 900 td average, 0.60 contrast). (c) First-harmonic test amplitudes for data of responses shown in a (●) and b (○). Solid lines are fits of the equation given in the legend to Fig. 1.