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Benjamin L. White, Jozsef Fiser; Suppression Of Ongoing Neural Variability In The Primary Visual Cortex With Learning. Invest. Ophthalmol. Vis. Sci. 2011;52(14):6098.
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© ARVO (1962-2015); The Authors (2016-present)
Neural responses to repeated presentations of identical sensory stimuli are highly variable. This widespread observation calls into question what information neuronal activity carries about sensory stimuli. Ongoing, spontaneous activity is highly variable, is known to reflect the animal’s state, and is a major contributor to stimulus response variability. We hypothesized that specific changes in an animal’s brain state due to associative learning would reduce the variability of ongoing activity in the primary visual cortex (V1) at specific times.
We used chronically-implanted bundles of microwire electrodes to record extracellular activity from V1 neurons of the rat during an associative learning. Rats were head fixed inside a light- and sound-attenuating chamber with a monitor 6 inches in front of the eyes, and a two-tastant delivery system with a lick sensor placed in front of the mouth. Rats were water restricted and trained to associate visual cues with liquid reinforcement. Specifically, the animals learned to expect a 1-second delayed sucrose solution (positive reinforcement) or a 1-second delayed quinine solution (negative reinforcement), depending on which of two visual cues were shown. Both visual cues were presented at randomized inter-stimulus time intervals and were identical in their overall size, luminance, and display time. Rats learned this task such that their lick rate was significantly higher just after the sucrose cue (but before reward delivery) than it was before the sucrose cue or after the quinine cue (but before quinine delivery).
We analyzed the spike trains from neurons in V1 in 1 second periods before, during and after visual cue onset. We found that neural variability across trials, as assessed by the fano factor, was significantly reduced from the spontaneous period before the sucrose cue to the spontaneous period after the sucrose cue. This effect was not observed for the periods around the quinine cue, and was also not observed for either cue before the rat’s licking behavior improved.
Our results indicate that neural variability in V1 is selectively suppressed by an upcoming expected reward, and supports the idea that ongoing neural activity reflects behaviorally-relevant changes in an animal’s internal state, even in primary sensory areas of the cortex.
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