Abstract

The joint storage and reciprocal retrieval of leant associated signals are presumably encoded by associative memory cells. In the accumulation and enrichment of memory contents in lifespan, a signal often becomes a core signal associatively shared for other signals. One specific group of associative memory neurons that encode this core signal likely interconnects multiple groups of associative memory neurons that encode these other signals for their joint storage and reciprocal retrieval. We have examined this hypothesis in a mouse model of associative learning by pairing the whisker tactile signal sequentially with the olfactory signal, the gustatory signal and the tail-heating signal. Mice experienced this associative learning show the whisker fluctuation induced by olfactory, gustatory and tail-heating signals, or the other way around, i.e., memories to multi-modal associated signals featured by their reciprocal retrievals. Barrel cortical neurons in these mice become able to encode olfactory, gustatory and tail-heating signals alongside the whisker signal. Barrel cortical neurons interconnect piriform, S1-Tr and gustatory cortical neurons. With the barrel cortex as the hub, the indirect activation occurs among piriform, gustatory and S1-Tr cortices for the second-order associative memory. These associative memory neurons recruited to encode multi-modal signals in the barrel cortex for associative memory are downregulated by neuroligin-3 knockdown. Thus, associative memory neurons can be recruited as the core cellular substrate to memorize multiple associated signals for the first-order and the second-order of associative memories by neuroligin-3-mediated synapse formation, which constitutes neuronal substrates of cognitive activities in the field of memoriology. HighlightO_LIThe coactivity of cerebral cortices during associative learning induces their interconnections. C_LIO_LIInterconnections endorse the first order and the second order of associative memory. C_LIO_LIAssociative memory cells in cerebral cortices are recruited by mutual synapse innervations. C_LIO_LINeuroligin-3 mediates the recruitment of associative memory cells for associative memory. C_LI