UC San Diego

Under the longstanding model of the primate primary visual cortex (V1), color and form are processed by distinct neurons that are clustered according to cytochrome oxidase (CO) expression. Previous studies have demonstrated that there is not strict spatial segregation but have continued to support the model at single neuron level; previous studies have failed to identify neurons selective for both orientation and color that respond much more strongly to their preferred color (on an equiluminant background) than to achromatic stimuli. But previous studies have been limited in their spatial resolution and sampling of stimulus space, leaving several outstanding questions.

We overcame limitations of previous studies by utilizing GCaMP6f 2-photon calcium imaging, which enabled long-term recording from large populations of neurons with single neuron resolution. We displayed a variety of stimuli, including equiluminant colored gratings and luminance-modulated achromatic gratings at a variety of orientations and spatial frequencies. We also conducted reverse correlation using cone-isolating gratings to map the cone inputs individual neurons. Finally, we aligned our calcium imaging results with intrinsic signal imaging (ISI) and postmortem histology to relate the responses of individual neurons to functional and anatomical markers, such as CO blobs.

We reveal that nearly half (46.4%) of neurons in V1’s superficial (cortico-cortical output) layers prefer colored to achromatic stimuli and nearly one-fifth (19.1%) respond more than twice as strongly to colored stimuli. Amongst these strongly color-preferring cells, the majority (11.6% of all cells) are also strongly orientation selective and located far from CO blobs, while the remaining color-preferring cells (7.5% of all cells) are poorly tuned for orientation and located close to CO blobs. We also reveal that cells are spatially organized according to preferred color and the sign of their dominant cone inputs.

These findings demonstrate that color and form are jointly processed by a previously unreported population of neurons located predominantly in the interblobs of primate V1, indicating that early and integrated processing contributes to perception of visual objects. Observations that both cone inputs and preferred hues are systematically mapped within V1 are likely to reflect underlying organization of thalamic inputs and local circuits within V1.