A possible coding for experience: ripple-like events and synaptic diversity

The hippocampal CA1 is necessary to maintain experienced episodic memory in many species, including humans. To monitor the temporal dynamics of processing, we recorded multiple-unit firings of CA1 neurons in male rats experiencing one of four episodes for 10 min: restraint stress, social interaction with a female or male, or observation of a novel object. Before an experience, the neurons mostly exhibited sporadic firings with some synchronized (≈ 50 ms) ripple-like firing events in habituated home cage. After experience onset, restraint or social interaction with other rats induced spontaneous high-frequency firings (super bursts) intermittently, while object observation induced the events inconsistently. Minutes after experience initiation, CA1 neurons frequently exhibited ripple-like firings with less-firing silent periods. The number of ripple-like events depended on the episode experienced and correlated with the total duration of super bursts. Experience clearly diversified multiple features of individual ripple-like events in an episode-specific manner, sustained for more than 30 min in the home cage. Ex vivo patch clamp analysis further revealed experience-promoted synaptic plasticity. Compared with unexposed controls, animals experiencing the female, male, or restraint episodes showed cell-dependently increased AMPA- or GABA A receptor– mediated postsynaptic currents, whereas contact with a novel object increased only GABAergic currents. Multivariate ANOVA in multi-dimensional virtual space revealed experience-specific super bursts with subsequent ripple-like events and synaptic plasticity, leading us to hypothesize that these factors are responsible for creating experience-specific memory. It is possible to decipher encrypted experience through the deep learning of the orchestrated ripple-like firings and synaptic plasticity in multiple CA1 neurons.