title: Memory formation and retrieval of neuronal silencing in the auditory cortex.
abstract: 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.
authors.affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan; h-nomu@umin.ac.jp.
authors.forename: Hiroshi
authors.initials: H
authors.lastname: Nomura
authors.affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan;
authors.forename: Kojiro
authors.initials: K
authors.lastname: Hara
authors.affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan;
authors.forename: Reimi
authors.initials: R
authors.lastname: Abe
authors.affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan;
authors.forename: Natsuko
authors.initials: N
authors.lastname: Hitora-Imamura
authors.affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan;
authors.forename: Ryota
authors.initials: R
authors.lastname: Nakayama
authors.affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan;
authors.forename: Takuya
authors.initials: T
authors.lastname: Sasaki
authors.affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan;
authors.forename: Norio
authors.initials: N
authors.lastname: Matsuki
authors.affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan; Center for Information and Neural Networks, National Institute of Information and Communications Technology, Osaka 565-0871, Japan.
authors.forename: Yuji
authors.identifier: http://orcid.org/0000-0003-2260-8191
authors.initials: Y
authors.lastname: Ikegaya
mesh_terms: D000818:Animals; D019843:Archaeal Proteins / Q000378:metabolism; D001245:Association Learning / Q000528:radiation effects; D001303:Auditory Cortex / Q000502:physiology* / Q000528:radiation effects; D003214:Conditioning, Classical / Q000528:radiation effects; D005239:Fear / Q000502:physiology; D046352:Freezing Reaction, Cataleptic / Q000528:radiation effects; D008027:Light; D008297:Male; D011939:Mental Recall / Q000502:physiology*; D008810:Mice, Inbred C57BL; D009474:Neurons / Q000502:physiology* / Q000528:radiation effects; D062308:Optogenetics; D012201:Reward; D014162:Transfection; D017494:Proton Pumps
chemical_list: D019843:Archaeal Proteins; C055476:archaerhodopsin protein, Archaea; D017494:Proton Pumps
keywords: auditory cortex; fear conditioning; neuronal inhibition; operant conditioning; optogenetics