A shared neural ensemble links distinct contextual memories encoded close in time

By Denise J. Cai, Daniel Aharoni, Tristan Shuman, Justin L. Shobe, Jeremy S. Biane, Weilin Song, Brandon Wei, Michael Veshkini, Mimi Q. La-Vu, Jerry Lou and 11 more. Nature, 2016

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A similar neural ensemble participates in the encoding of two distinct memories, resulting in the recall of one memory increasing the likelihood of recalling the other, but only if those memories occur very closely in time—within a day rather than across a week. This paper tests and provides support for the emerging hypothesis that two distinct memories formed close in time may be linked, such that recall of one triggers recall of the other. Using a range of techniques including in vivo calcium imaging with miniature head-mounted fluorescent microscopes in freely behaving mice, Alcino Silva and colleagues show that learning-dependent changes in excitability can temporally and contextually link memories formed close in time. Interestingly the overlap between memory encoding ensembles and strengthening of the second memory within short periods of time do not occur in aged animals, which do not exhibit the increased hippocampal excitability necessary for such links to occur. Recent studies suggest that a shared neural ensemble may link distinct memories encoded close in time1,2,3,4,5,6,7,8,9,10,11,12. According to the memory allocation hypothesis1,2, learning triggers a temporary increase in neuronal excitability13,14,15 that biases the representation of a subsequent memory to the neuronal ensemble encoding the first memory, such that recall of one memory increases the likelihood of recalling the other memory. Here we show in mice that the overlap between the hippocampal CA1 ensembles activated by two distinct contexts acquired within a day is higher than when they are separated by a week. Several findings indicate that this overlap of neuronal ensembles links two contextual memories. First, fear paired with one context is transferred to a neutral context when the two contexts are acquired within a day but not across a week. Second, the first memory strengthens the second memory within a day but not across a week. Older mice, known to have lower CA1 excitability15,16, do not show the overlap between ensembles, the transfer of fear between contexts, or the strengthening of the second memory. Finally, in aged mice, increasing cellular excitability and activating a common ensemble of CA1 neurons during two distinct context exposures rescued the deficit in linking memories. Taken together, these findings demonstrate that contextual memories encoded close in time are linked by directing storage into overlapping ensembles. Alteration of these processes by ageing could affect the temporal structure of memories, thus impairing efficient recall of related information.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/ceeaffd07b8839fa5f685c5f71b0d64da746d6bc

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Citations in the corpus

Differential conditioning produces merged long-term memory in Drosophila (2021, background): “, 2018; Kahana, 1996), and the memory allocation phenomenon observed in rodents (Cai et al., 2016; Rashid et al., 2016).”
Memory engrams: Recalling the past and imagining the future (2020, background): “Similarly, coallocation of CA1 engram cells supporting memories of two distinct contexts was observed if exposure to the contexts was separated by a short time interval (216).”
Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data (2018, neutral): “This technique has been widely used to study the neural circuits in cortical, subcortical, and deep brain areas, such as hippocampus (Cai et al., 2016; Ziv et al., 2013; Jimenez et al., 2018; Rubin et al., 2015), entorhinal cortex (Kitamura et al., 2015; Sun et al., 2015), hypothalamus (Jennings et…”
Loss of Ensemble Segregation in Dentate Gyrus, but not in Somatosensory Cortex, during Contextual Fear Memory Generalization (2016, methodology): “In our current study and previous reports (Reijmers et al., 2007; Deng et al., 2013; Cai et al., 2016), instead of endogenous c-Fos, ZIF was used as an activity marker of neurons activated during retrieval test.”
Tracking the Same Neurons across Multiple Days in Ca2+ Imaging Data (2017, methodology): “…in head-fixed rodents (Dombeck et al., 2007, 2010; Kitamura et al., 2015; Burgess et al., 2016) or onephoton imaging with miniature microscopes in freely behaving rodents (Ziv et al., 2013; Berdyyeva et al., 2014; Jennings et al., 2015; Pinto and Dan, 2015; Sun et al., 2015; Cai et al., 2016).”
CaImAn an open source tool for scalable calcium imaging data analysis (2019, methodology): “A typical resonant scanning two-photon microscope produces data at a rate greater than 50 GB/Hr (calculation performed on a 512 512 Field of View imaged at 30 Hz producing an unsigned 16-bit integer for each measurement), a number that can be significantly higher (up to more than 1TB/Hour) with othe”