Robust population orientation encoding by orientation-untuned neurons in macaque V1

Abstract Orientation is one of the most fundamental stimulus features in visual perception. In the primary visual cortex (V1), while most neurons are orientation-selective, a small portion exhibits a lack of this selectivity. However, it remains unclear what roles the orientation-untuned V1 neurons play in population orientation discrimination. Here, we analyzed data from a 2-photon calcium imaging study that recorded the responses of thousands of V1 neurons to a grating stimulus at various orientations in awake macaques. Our population analysis reveals that orientation-untuned neurons can independently decode stimulus orientation with accuracy comparable to tuned neurons. Remarkably, we found that the more critical role of orientation-untuned neuronal populations in orientation encoding is to enhance coding robustness, specifically by reducing sensitivity to noise. Moreover, when using artificial neural networks to model the primate ventral visual pathway, we found that the V1-like layer also contains a proportion of orientation-untuned units. Removing these units leads to significant impairments in natural object recognition. Overall, these results indicate that orientation-untuned neurons encode orientation information and play a crucial role in primate visual perception. The study provides compelling evidence for a continuous distribution of visual features across neurons and challenges the notion of highly specialized units.