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After the integrative storage of associated signals, a signal induces the recollection of its associated signal, or the other way around. This associative memory is essential to associative thinking, logical reasoning, imagination and computation. In terms of cellular mechanisms underlying associative memory, new mutual synapse innervations are formed among those coactivated neurons, so that they are recruited to be associative memory cells or associative memory neurons. These associative memory cells receive new synapse innervations alongside innate synapse inputs and encode signals carried by these inputs. We proposed to examine microRNAs as initiative factors for recruiting new synapse innervations and associative memory cells. In a mouse model of associative memory characterized as the reciprocal retrieval of associated whisker and odor signals, barrel and piriform cortical neurons gain their ability to encode whisker and odorant signals based on the newly formed synapse innervations between these coactivated cortices besides innate synapse inputs. miRNA-324 and miRNA-133a are required for recruiting these new synapse innervations and associative memory cells as well as sufficient for facilitating their recruitments, but not for innate synapse inputs. Therefore, the coactivation of sensory cortices through microRNA as initiative factor to recruit new mutual synapse innervations and associative memory cells for associative memory., (Copyright © 2020 Elsevier Inc. All rights reserved.)

After associative learning, a signal induces the recall of its associated signal, or the other way around. This reciprocal retrieval of associated signals is essential for associative thinking and logical reasoning. For the cellular mechanism underlying this associative memory, we hypothesized that the formation of synapse innervations among coactivated sensory cortices and the recruitment of associative memory cells were involved in the integrative storage and reciprocal retrieval of associated signals. Our study indicated that the paired whisker and olfaction stimulations led to an odorant-induced whisker motion and a whisker-induced olfaction response, a reciprocal form of associative memory retrieval. In mice that showed the reciprocal retrieval of associated signals, their barrel and piriform cortical neurons became mutually innervated through their axon projection and new synapse formation. These piriform and barrel cortical neurons gained the ability to encode both whisker and olfaction signals based on synapse innervations from the innate input and the newly formed input. Therefore, the associated activation of sensory cortices by pairing input signals initiates their mutual synapse innervations, and the neurons innervated by new and innate synapses are recruited to be associative memory cells that encode these associated signals. Mutual synapse innervations among sensory cortices to recruit associative memory cells may compose the primary foundation for the integrative storage and reciprocal retrieval of associated signals. Our study also reveals that new synapses onto the neurons enable these neurons to encode memories to new specific signals., (Copyright © 2019 Elsevier B.V. All rights reserved.)