Published in Annual Meeting, Neuroscience, Oct 2015.
Visual experience relies in large part on our ability to appreciate subtle differences in the orientation of visual features. In primates, selectivity for orientation emerges in primary visual cortex (V1) and is also common in downstream cortical areas such as V2. We investigated the relation between single cell activity in macaque V1 and V2 and simultaneously measured psychophysical judgments of stimulus orientation. We trained two macaque monkeys to discriminate the orientation of drifting gratings presented for 500 ms in the near periphery. To enable a direct comparison of neuronal and behavioral sensitivity, we tailored the stimulus (grating size, scale, and speed) and task (the orientations to be discriminated) to the tuning properties of the neuron under study. Both animals performed the task well, with thresholds that varied between 1 and 5 deg for a wide range of stimulus conditions (mean threshold: 3.3 deg and 2.8 deg, respectively). Ideal observer analysis of neuronal responses revealed that single V1 and V2 neurons carried almost as much information about stimulus orientation as the animals' behavioral reports. On average, psychophysical sensitivity exceeded neuronal sensitivity by 65% in V1 and 45% in V2. We also estimated "choice probability": the degree to which fluctuations in neural activity predict fluctuations in behavioral judgments across repeated presentations of the same stimulus. Although both monkeys had similar behavioral sensitivity, choice probability differed between animals. For one monkey, there was no systematic choice-related activity evident in the responses of V1 or V2 neurons. For the other, there was a weak but systematic choice probability. However, the sign of this relationship was, unexpectedly, negative: when an orientation-selective neuron fired more spikes, the animal was less likely to make a decision in favor of the orientation preferred by the neuron. Our results suggest that single cell sensitivity in V1 imposes an upper bound on behavioral sensitivity for fine orientation discrimination, and that the component of neuronal variability that gives rise to choice-related activity in sensory neurons is divorced from the component that limits behavioral sensitivity.