Blue-yellow opponency in primate S cone photoreceptors

Abstract

The neural coding of human color vision begins in the retina. The outputs of long (L)-, middle (M)-, and short (S)-wavelength-sensitive cone photoreceptors combine antagonistically to produce "red-green" and "blue-yellow" spectrally opponent signals (Hering, 1878; Hurvich and Jameson, 1957). Spectral opponency is well established in primate retinal ganglion cells (Reid and Shapley, 1992; Dacey and Lee, 1994; Dacey et al., 1996), but the retinal circuitry creating the opponency remains uncertain. Here we find, from whole-cell recordings of photoreceptors in macaque monkey, that "blue-yellow" opponency is already present in the center-surround receptive fields of S cones. The inward current evoked by blue light derives from phototransduction within the outer segment of the S cone. The outward current evoked by yellow light is caused by feedback from horizontal cells that are driven by surrounding L and M cones. Stimulation of the surround modulates calcium conductance in the center S cone.

Figure 1.

S cone identification. A, Infrared image of retina focused on rod (small) and cone (large) inner segments. Arrow indicates S cone. B, Membrane current response to cone-isolating stimuli. Colored lines plot photoisomerization/s (R*/s) in L (red), M (green), and S (blue) cones. C, Top: Concatenated responses to increasing spatial frequencies. Bottom: Response amplitude (symbols) versus spatial frequency from 3 S cones. Lines plot Equation 1 with λ = 1.9 (•), 4.1 (▵), and 2.8 (■) μm. Membrane potential −60 mV. S cone sinusoidal modulated stimulus with mean photoisomerizations/s of 1.6 × 10⁶, 1.2 × 10⁶, and 5.9 × 10⁵ in L, M, and S cones, respectively. S cone Michelson contrast 94%.

Figure 2.

S cone chromatic opponency is created by horizontal cell feedback. A, Short-wavelength blue light evokes outward current; long-wavelength yellow light evokes inward current. B, Inward current evoked by yellow light is blocked by 20 μm CNQX. A, B, Membrane potential voltage-clamped at −40 mV. Stimulus monitor below current traces. Photoisomerizations/s in L, M, and S cones, respectively, are: 1.2 × 10⁶, 2.0 × 10⁶, and 4.3 × 10⁶ (blue), and 2.8 × 10⁶, 1.8 × 10⁶, and 1.9 × 10³ (yellow).

Figure 3.

Opponent surround activates calcium currents. A, Voltage-activated calcium currents increased in steady yellow light. Membrane potential stepped from –70 mV to between −85 and −5 mV. Responses shown for steps to between −50 and −30 mV. Voltage monitor above current traces. Calcium currents were isolated by including Cs and TEA in the patch solution (see Materials and Methods) and by subtraction of the capacitance and linear leak currents. Dark measurements were averaged from records before and after each light measurement. B, Peak change in membrane current in dark (•) and light (○) versus voltage. Points averaged across 7 trials from 3 cones; bars indicate SDs. C, Light–dark difference of calcium currents. A–C, Light evoked 2.8 × 10⁶, 1.8 × 10⁶, and 1.9 × 10³ photoisomerizations/s in the L, M, and S cones.

Figure 4.

Size of opponent surround. A, Responses to flashed annuli; inner radius 25–500 μm, outer radius 1 mm. Flash monitor above current traces. B, Peak response amplitude versus inner radius from 4 cones. Annular flash: Long-wavelength flash from darkness (□, ■, ▵) evoked 3.5 × 10⁶, 2.6 × 10⁶, and 1.1 × 10⁵ photoisomerizations/s in L, M, and S cones, or L+M cone modulation (•), with background rate of ∼1.5 × 10⁵ photoisomerizations/s for L, M, and S cones and a flashed increment of 5.7 × 10⁶ (L), 5.6 × 10⁶ (M), and 0 (S). Membrane potential −40 mV. Lines are Equation 2 with λ_S = 172 (□), 176 (■), 180 (▵), or 140 (•) μm.