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Memory formation and retrieval of neuronal silencing in the auditory cortex

Significance Cortical neurons exhibit spontaneous activity without explicit external stimuli. Sensory stimuli not only activate specific populations of those neurons but can also silence other populations. However, it remains unclear whether neuronal silencing per se leads to memory formation and behavioral expression. Here, we used optogenetic silencing of a neuronal ensemble in the auditory cortex and found that mice exhibited a fear response to silencing that had been previously paired with footshock, and could find a reward based on the presence or absence of the silencing. These findings indicate that neuronal silencing per se, which is originally believed to be involved in neuronal modulation, is enough to elicit a cognitive behavior. Sensory stimuli not only activate specific populations of cortical neurons but can also silence other populations. However, it remains unclear whether neuronal silencing per se leads to memory formation and behavioral expression. Here we show that mice can report optogenetic inactivation of auditory neuron ensembles by exhibiting fear responses or seeking a reward. Mice receiving pairings of footshock and silencing of a neuronal ensemble exhibited a fear response selectively to the subsequent silencing of the same ensemble. The valence of the neuronal silencing was preserved for at least 30 d and was susceptible to extinction training. When we silenced an ensemble in one side of auditory cortex for conditioning, silencing of an ensemble in another side induced no fear response. We also found that mice can find a reward based on the presence or absence of the silencing. Neuronal silencing was stored as working memory. Taken together, we propose that neuronal silencing without explicit activation in the cerebral cortex is enough to elicit a cognitive behavior.