Orientation discrimination requires coactivation of on- and off-dominated visual channels

Orientation sensitivity depends on the cortical convergence of on- and off-center subcortical neurons. Off-center inputs are faster and stronger than their on-center counterparts: How does this asymmetry affect orientation discrimination? We tackled this question psychophysically with grating stimuli that either increased or decreased luminance. The gratings were of low contrast in order to avoid the complicating influences of nonlinearities such as response saturation, masking, and aftereffects. Gratings were presented in either of two locations, and subjects indicated the perceived location. Stimuli were randomly timed, and response correctness and reaction time were recorded. We found the following: (a) Contrast sensitivity was insignificant for a range of contrasts around zero. (b) Outside this range, contrast sensitivity for contrast decrements exceeded that for increments by an average of 15%. (c) Reaction times for contrast decrements were up to 45 ms less than for increments. (d) These findings are reproduced by a signal-detection model which incorporates recent physiological findings: Neurons in primary visual cortex are hyperpolarized at rest; these neurons respond more to darks than to lights; and off-dominated cortical neurons have shorter latencies than their on-dominated neighbors. (e) We tested orientation discrimination by splitting a grating into two components, one containing the light bars and the other the dark, and presenting the two components asynchronously. Discrimination was optimal when light bars preceded dark bars, consistent with coactivation of on- and off-center cortical inputs. We conclude that the ability to discriminate between orientations is intimately connected with the properties of subcortical channels.