Date Published: July 25, 2019
Publisher: Public Library of Science
Author(s): Brian P. Schmidt, Alexandra E. Boehm, William S. Tuten, Austin Roorda, Daniel Osorio.
The human retina contains three classes of cone photoreceptors each sensitive to different portions of the visual spectrum: long (L), medium (M) and short (S) wavelengths. Color information is computed by downstream neurons that compare relative activity across the three cone types. How cone signals are combined at a cellular scale has been more difficult to resolve. This is especially true near the fovea, where spectrally-opponent neurons in the parvocellular pathway draw excitatory input from a single cone and thus even the smallest stimulus projected through natural optics will engage multiple color-signaling neurons. We used an adaptive optics microstimulator to target individual and pairs of cones with light. Consistent with prior work, we found that color percepts elicited from individual cones were predicted by their spectral sensitivity, although there was considerable variability even between cones within the same spectral class. The appearance of spots targeted at two cones were predicted by an average of their individual activations. However, two cones of the same subclass elicited percepts that were systematically more saturated than predicted by an average. Together, these observations suggest both spectral opponency and prior experience influence the appearance of small spots.
A central goal of neuroscience is to understand how signals from sensory receptors are transformed into perceptual experience. In vision, photoreceptor cells in the retina encode real-time information about light in the environment. However, the signals conveyed by individual photoreceptors are noisy and ambiguous. A well-known example can be found in color vision. The spectral signals carried by individual cones are inherently ambiguous because each cone type is responsive to a relatively broad portion of the visible spectrum. As a result, a given magnitude of photoreceptor activity could result from virtually any combination of stimulus wavelength and intensity . To extract color information from the photoreceptor mosaic, color-opponent neurons must compare the relative activity between cones with different spectral sensitivities [2–4]. Once a census of activity in the three cone types has been taken, the brain constructs a percept by inferring which stimulus most likely produced that activity pattern. In everyday viewing, our visual system navigates this process effortlessly, presumably by exploiting statistical regularities in the spatial, temporal and chromatic structure of natural images it has learned through experience.
The goal of these experiments was to determine how the visual system combines information across cones when making color judgments. To investigate this question, we probed L- and M-cones individually or in pairs with an AOSLO microstimulator. Before quantifying color appearance, we first measured detection thresholds in the one and two cone conditions and scaled our stimuli accordingly to ensure equal detectability across conditions. During appearance experiments, we used these measurements to set the stimulus energy level to achieve 85% frequency of seeing in both the one- and two-cone conditions.
We quantified the color appearance of small spots of light targeted to individual or pairs of cones. Our experiments revealed that both the number and spectral type of targeted cones influenced color reports (Fig 2). Generally, pairs of cones elicited colored percepts that were predicted by an average of individual responses (Fig 3). This finding suggests that each cone contributes to the post-receptoral circuits involved in color vision and is inconsistent with the view that a subgroup of cones are the sole stakeholders in the processes responsible for generating hue sensations.