Relationship between the local structure of orientation map and the strength of orientation tuning of neurons in monkey V1: a 2-photon calcium imaging study.

A majority of neurons in the monkey primary visual cortex (V1) are tuned to stimulus orientations. Preferred orientations and tuning strengths vary among V1 neurons. The preferred orientation of neurons gradually changes across the cortex with occasional failures of this organization. How V1 neurons are arranged by the strength of orientation tuning and whether neuronal arrangement for tuning strength relates to orientation preference maps remains controversial. In this study, we performed in vivo two-photon calcium imaging in macaque V1 to examine the local spatial organization of orientation tuning at the level of single cells. We recorded fluorescence signals from individual neurons loaded with a calcium-sensitive dye in layer 2 and the uppermost tier of layer 3. The strength of orientation tuning was shared by nearby neurons, and changed across the cortex. The neurons with similar tuning strength were distributed across at least the entire thickness of layer 2. The tuning strength was weaker in regions where neurons exhibited heterogeneous preferred orientations, as compared with regions where neurons shared similar orientation preferences. Nearby direction-selective neurons often shared their preferred directions, although only a few neurons were direction selective in the layers examined. Thus, the orientation tuning strength of V1 neurons is partially predictable from the local structure of orientation map. The weaker orientation tuning we found in regions with heterogeneous orientation preferences suggests that orientation-independent interactions among local populations of V1 neurons play a critical role in determining their orientation tuning.