<i>Alouatta</i> Trichromatic Color Vision: Cone Spectra and Physiological Responses Studied with Microspectrophotometry and Single Unit Retinal Electrophysiology

<div><p>The howler monkeys (<i>Alouatta</i> sp.) are the only New World primates to exhibit routine trichromacy. Both males and females have three cone photopigments. However, in contrast to Old World monkeys, <i>Alouatta</i> has a locus control region upstream of each opsin gene on the X-chromosome and this might influence the retinal organization underlying its color vision. Post-mortem microspectrophotometry (MSP) was performed on the retinae of two male <i>Alouatta</i> to obtain rod and cone spectral sensitivities. The MSP data were consistent with only a single opsin being expressed in each cone and electrophysiological data were consistent with this primate expressing full trichromacy. To study the physiological organization of the retina underlying <i>Alouatta</i> trichromacy, we recorded from retinal ganglion cells of the same animals used for MSP measurements with a variety of achromatic and chromatic stimulus protocols. We found MC cells and PC cells in the <i>Alouatta</i> retina with similar properties to those previously found in the retina of other trichromatic primates. MC cells showed strong phasic responses to luminance changes and little response to chromatic pulses. PC cells showed strong tonic response to chromatic changes and small tonic response to luminance changes. Responses to other stimulus protocols (flicker photometry; changing the relative phase of red and green modulated lights; temporal modulation transfer functions) were also similar to those recorded in other trichromatic primates. MC cells also showed a pronounced frequency double response to chromatic modulation, and with luminance modulation response saturation accompanied by a phase advance between 10–20 Hz, characteristic of a contrast gain mechanism. This indicates a very similar retinal organization to Old-World monkeys. Cone-specific opsin expression in the presence of a locus control region for each opsin may call into question the hypothesis that this region exclusively controls opsin expression.</p></div

Ganglion cell response to stimulus phase changes.

<p>(<b>A</b>) MC and (<b>B</b>) PC cell responses to heterochromatic stimuli. Phase protocol. The relative phases of the 554 and 638 nm LEDs were modulated with fixed modulation depths. MC and PC cells were stimulated at 9.8 Hz and 1.22 Hz, respectively. Stimulus size was 4 deg, mean retinal illuminance was 2000 Td. Response amplitudes (top panels) and phases (middle panels) are shown as a function of the phase difference between the luminance modulation in the red and green LEDs. Filled diamonds and empty squares represent the parameters for response first and second harmonics, respectively, extracted by Fourier analysis. Bottom panels: the histograms illustrate actual responses to two cycles of modulation, the arrows indicate the red/green phase difference for the histograms, and the red and green curves represent how the phase of the red and green lights changed for each stimulus condition. Luminance modulation corresponds to a relative phase of 0 deg, chromatic modulation to a relative phase of ±180 deg. MC cells responded to the phase protocol with a maximal response first harmonic amplitude when the green and red lights were modulated in phase and their response phase changed continuously with the phase difference between the modulation in the two LEDs. PC cells displayed a minimal response when the green and red lights were modulated in phase and their response phases changed abruptly in the region of minimal response.</p

Ganglion cell response to stimulus contrast.

<p>(<b>A–B</b>) Response amplitude (left panels) and phase (right panels) as a function of stimulus luminance contrast for <i>Alouatta</i> MC cell (<b>A</b>) and PC cell (<b>B</b>). The results obtained with three temporal frequencies are given: 1.2 Hz (filled squares), 9.8 Hz (filled triangles), and 39 Hz (filled diamonds) for the MC cell; 1.2 Hz (filled squares), 9.8 Hz (filled triangles), and 19.4 Hz (filled diamonds) for the PC cell. Data representing response amplitude as a function of contrast have been fitted with Naka-Rushton functions. MC cell vigorously responded to low levels of luminance contrast, but responses rapidly saturated accompanied by advancement in response phase, especially at intermediate and high temporal frequencies. PC cells were quite insensitive to low levels of luminance contrast, but the responses did not exhibit saturation or phase advancement. (<b>C</b>) Temporal modulation transfer functions (temporal MTFs) for <i>Alouatta</i> MC cells (average of 7 cells) stimulated with luminance sinusoids (filled squares) and a PC cell stimulated with luminance (empty diamonds) and averaged responses of 4 cells to red-green (filled diamonds) sinusoids. Contrast gain was defined as the initial slope of the Naka-Rushton functions fitted to the amplitude versus contrast data such as those illustrated in the left panels (<b>A–B</b>). Michelson contrast and cone contrast were used for the luminance and red-green chromatic temporal MTFs, respectively. MC cells were much more sensitive than PC cells to temporal luminance modulation at all the temporal frequencies range and vigorously responded to very high temporal frequencies. On the other hand, PC cells were very sensitive to red-green contrast, especially at low and intermediate temporal frequencies.</p