Contribution of non-sensory neurons in visual cortical areas to visually guided decisions in the rat

It is widely assumed that trial-by-trial variability in visual detection performance is explained by the fidelity of visual responses in visual cortical areas influenced by fluctuations of internal states, such as vigilance and behavioral history. However, it is not clear which neuronal ensembles represent such different internal states. Here, we utilized a visual detection task, which distinguishes internal states in response to identical stimuli, while recording neurons simultaneously from the primary visual cortex (V1) and the posterior parietal cortex (PPC). We found that rats sometimes withheld their responses to visual stimuli despite the robust presence of visual responses in V1. Our unsupervised analysis revealed distinct population dynamics segregating hit responses from misses, orthogonally embedded to visual response dynamics in both V1 and PPC. Heterogeneous non-sensory neurons in V1 and PPC significantly contributed to population-level encoding accompanied with the modulation of noise correlation only in V1. These results highlight the non-trivial contributions of non-sensory neurons in V1 and PPC for population-level computations that reflect the animals’ internal states to drive behavioral responses to visual stimuli. [Display omitted] •Rats often fail to respond to visual stimuli despite the presence of V1 responses•State fluctuation, but not visual response, correlates with visual detection•Stimulus non-preferring neurons in V1 and PPC contribute to state fluctuation•Stimulus timing relative to state fluctuations in V1 correlates with decision bias The trial-by-trial variability in visual detection performance can be attributed to the neural state fluctuations in visual cortical areas. Osako et al. show that stimulus timing relative to the state of the non-sensory neurons in the visual cortical areas segregates visual detection performance via the population-level mechanism.