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Abstract Visual cortical responses are known to be highly variable across trials within an experimental session. However, the long-term stability of visual cortical responses is poorly understood. Here using chronic imaging of V1 in mice we show that neural responses to repeated natural movie clips are unstable across weeks. Individual neuronal responses consist of sparse episodic activity which are stable in time but unstable in gain across weeks. Further, we find that the individual episode, instead of neuron, serves as the basic unit of the week-to-week fluctuation. To investigate how population activity encodes the stimulus, we extract a stable one-dimensional representation of the time in the natural movie, using an unsupervised method. Most week-to-week fluctuation is perpendicular to the stimulus encoding direction, thus leaving the stimulus representation largely unaffected. We propose that precise episodic activity with coordinated gain changes are keys to maintain a stable stimulus representation in V1. 

Both experimenter-controlled stimuli and stimulus-independent variables impact cortical neural activity. A major hurdle to understanding neural representation is distinguishing between qualitatively different causes of the fluctuating population activity. We applied an unsupervised low-rank tensor decomposition analysis to the recorded population activity in the visual cortex of awake mice in response to repeated presentations of naturalistic visual stimuli. We found that neurons covaried largely independently of individual neuron stimulus response reliability and thus encoded both stimulus-driven and stimulus-independent variables. Importantly, a neuron’s response reliability and the neuronal coactivation patterns substantially reorganized for different external visual inputs. Analysis of recurrent balanced neural network models revealed that both the stimulus specificity and the mixed encoding of qualitatively different variables can arise from clustered external inputs. These results establish that coactive neurons with diverse response reliability mediate a mixed representation of stimulus-driven and stimulus-independent variables in the visual cortex. NEW & NOTEWORTHY V1 neurons covary largely independently of individual neuron’s response reliability. A single neuron’s response reliability imposes only a weak constraint on its encoding capabilities. Visual stimulus instructs a neuron’s reliability and coactivation pattern. Network models revealed using clustered external inputs.