Associative Memory Cells are Recruited to Encode Triple Sensory Signals via Synapse Formation

Abstract

Associative learning is a common form of information acquisition, and associative memory is essential for logical reasoning and associative thinking. In addition to memory cells for two associated signals, here we report the recruitment of associative memory cells that encode triple sensory signals. Paired mouse whisker, olfaction and tail stimulations lead to odorant-induced and tail-induced whisker motions. In the mice of showing cross-modal reflexes, barrel cortical neurons and astrocytes become to encode odor and tail signals alongside whisker signal. Such neurons receive the new synapse innervations from the axons of the piriform and S1-tail cortical neurons, in addition to the innate synapse innervations from the axons of the thalamic neurons. The formation of new synapse innervations and the recruitment of associative memory cells require the upregulations of miRNA-324-5p and miRNA-133a-3p that downregulate tau-tubulin kinase-1 (Ttbk1) and methylcytosine dioxygenase Tet3. The associated activations of the sensory cortices elicit their mutual synapse innervations that recruit memory cells to store triple associated signals via epigenetic processes. Furthermore, after the extinction of cross-modal reflexes, the refinements of the synapses and memory cells in the barrel cortex are well maintained, while plasticity in the M1-motor cortex decreases. These results indicate that the acquired signals remain stored in the sensory cortices and the decay of memory retrieval is due to the decreased refinement of their downstream cortical regions in neural circuits from the sensory cortices to the memory-presentation cortices. In terms of the significance of our discoveries, the storages of multiple signals in individual neurons may expand memory volumes, strengthen cognition capabilities and facilitate creative inspiration productions. Information storages in the sensory cortices confer them to signify the sources of the retrieved memory signals. This study is supported by National Basic Research Program (2013CB531304 and 2016YFC1307100) and Natural Science Foundation China (81671071 and 81471123) to JHW.