Abstract
One of the fundamental goals in neurosciences is to elucidate the formation and retrieval of brain's associative memory traces in real-time. Here, we describe real-time neural ensemble transient dynamics in the mouse hippocampal CA1 region and demonstrate their relationships with behavioral performances during both learning and recall. We employed the classic trace fear conditioning paradigm involving a neutral tone followed by a mild foot-shock 20 seconds later. Our large-scale recording and decoding methods revealed that conditioned tone responses and tone-shock association patterns were not present in CA1 during the first pairing, but emerged quickly after multiple pairings. These encoding patterns showed increased immediate-replay, correlating tightly with increased immediate-freezing during learning. Moreover, during contextual recall, these patterns reappeared in tandem six-to-fourteen times per minute, again correlating tightly with behavioral recall. Upon traced tone recall, while various fear memories were retrieved, the shock traces exhibited a unique recall-peak around the 20-second trace interval, further signifying the memory of time for the expected shock. Therefore, our study has revealed various real-time associative memory traces during learning and recall in CA1, and demonstrates that real-time memory traces can be decoded on a moment-to-moment basis over any single trial.
Highlights
What are neural population-level memories in real-time? Can we decode neural populations’ memory traces as the subjects form and recall memories? How meaningfully can real-time memory traces in the brain be related to a behavioral readout? These enduring questions have attracted a keen interest of many philosophers, psychologists, neuroscientists and beyond [1,2,3]
Our experiments started with a three-day habituation session prior to training, in which the mice were introduced to two distinct chambers (5 minutes in each chamber, per day)
Extensive behavioral and lesion studies show that the hippocampus is involved in both the encoding and retrieval of various associative memories, including trace fear conditioning memory [3,4,6,7,18,19,20,21,22,23]
Summary
What are neural population-level memories in real-time? Can we decode neural populations’ memory traces as the subjects form and recall memories? How meaningfully can real-time memory traces in the brain be related to a behavioral readout? These enduring questions have attracted a keen interest of many philosophers, psychologists, neuroscientists and beyond [1,2,3]. There are several variations in term of the nature of conditioned (tone, light, odor, etc) and unconditioned stimuli (mild electrical foot-shock, air-puff to eyelid, etc). These protocols can produce long-lasting associative memories in the brains of various animal species. It has been shown that this classical Pavlov conditioning induces increased neuronal discharges in the hippocampus and cerebellum [3,7,9,10,11] Such learning paradigms have been shown to produce changes in latency responses and membrane potentials [3,9,10,11,12,13,14,15]. The well-defined, salient nature of cues and memory produced by this classic conditioning test offers an excellent paradigm for search of the neural basis of memory traces [3]
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