Optogenetics has advanced our understanding of the neural basis of simple behaviors in rodents and small animals. In primates, however, for which more sophisticated behavioral assays exist, optogenetic manipulations of behavior have been unsuccessful. Here, we report that monkeys reliably shift their gaze toward the receptive field of optically driven channelrhodopsin–2–expressing V1 neurons. This result establishes optogenetics as a viable tool for the causal analysis of behavior in primate brain.
Chromatic sensitivity cannot exceed limits set by noise in the cone photoreceptors. To determine how close neurophysiological and psychophysical chromatic sensitivity come to these limits, we developed a parameter-free model of stimulus encoding in the cone outer segments, and we compared the sensitivity of the model to the psychophysical sensitivity of monkeys performing a detection task and to the sensitivity of individual V1 neurons. Modeled cones had a temporal impulse response and a noise power spectrum that were derived from in vitro recordings of macaque cones, and V1 recordings were made during performance of the detection task. The sensitivity of the simulated cone mosaic, the V1 neurons, and the monkeys were tightly yoked for low-spatiotemporal-frequency isoluminant modulations, indicating high-fidelity signal transmission for this class of stimuli. Under the conditions of our experiments and the assumptions for our model, the signal-to-noise ratio for these stimuli dropped by a factor of ∼3 between the cones and perception. Populations of weakly correlated V1 neurons narrowly exceeded the monkeys' chromatic sensitivity but fell well short of the cones' chromatic sensitivity, suggesting that most of the behavior-limiting noise lies between the cone outer segments and the output of V1. The sensitivity gap between the cones and behavior for achromatic stimuli was larger than for chromatic stimuli, indicating greater postreceptoral noise. The cone mosaic model provides a means to compare visual sensitivity across disparate stimuli and to identify sources of noise that limit visual sensitivity.
Spectral sensitivity of humans and rhesus monkeys was compared using identical displays and similar procedures. Detection thresholds were measured for the following: 1) 15-Hz modulation of a blue and a green cathode-ray tube phosphor; 2) 15-Hz modulation of all three phosphors together; and 3) slow (<1 Hz) modulations of a blue and a green phosphor under scotopic conditions. Monkeys had lower blue-to-green threshold ratios than humans at all eccentricities tested (0.5 to 7°), consistent with a lower lens optical density in monkeys. In addition to apparently having a lower lens density than humans, monkeys were more sensitive to 15-Hz red-green isoluminant modulations than humans, an effect that cannot be explained by optical factors.
Optogenetics has emerged as a powerful tool for studying the neural basis of simple behaviors in rodents and small animals. In the primate model, however, optogenetics has had limited utility because optical methods have not been able to drive behavior. Here, we report that monkeys reliably shift their gaze toward the receptive field of optically driven channelrhodopsin-2-expressing V1 neurons. This result establishes optogenetics as a viable means for the causal analysis of behavior in the primate model.
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