Cortical state and natural movie responses in cat visual cortex

How does cortical state affect neural responses to naturalistic stimuli, and is it analogous between anesthetized and awake animals? We recorded spikes and local field potential (LFP) from all layers of isoflurane-anesthetized cat primary visual cortex (V1) while repeatedly presenting wide-field natural scene movie clips. Spiking responses of single units were remarkably precise, reliable and sparse, with lognormally distributed mean firing rates. Many units had distinct barcode-like firing patterns, with features as little as 10 ms wide. LFP-derived cortical state switched spontaneously between synchronized (1/f) and desynchronized (broadband). Surprisingly, responses were more precise, reliable and sparse during the synchronized than desynchronized state. Because the desynchronized state under anesthesia is thought to correspond to attending periods in awake animals, during which responses are enhanced, our results complicate the analogy between cortical states in anesthetized and awake animals. The presenceof orientation maps in cat V1 may explain contrary reports in anesthetized rodents, and predicts a similar result in anesthetized ferret and primate V1.Significance StatementGlobal brain activity changes spontaneously over time and can be characterized along a spectrum from slow synchronized activity, to fast desynchronized activity. This spectrum is similar in awake, asleep and anesthetized animals, but is its effect on neural responses the same in all cases? Here we show that neural responses to natural movies in anesthetized cat visual cortex are more precise during synchronized activity. This is contrary to reports in anesthetized rodents, which we suggest may be due to greater columnar organization in cat visual cortex. Since this is also contrary to enhanced responses and behavioural performance during attention, when activity is desynchronized, our results suggest that similar brain states in awake and anesthetized animals may not be functionally analogous.