The hippocampal engram maps experience but not place

Tanaka, Kazumasa Z.; He, Hongshen; Tomar, Anupratap; Niisato, Kazue; Huang, Arthur; McHugh, Thomas J.

doi:10.1126/science.aat5397

Cited by 193 publications

(170 citation statements)

References 29 publications

(25 reference statements)

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“…94 We then quantified the relationship between calcium activity and IEG expression. Consistent with 95 previous reports (Tanaka et al, 2018;Yassin et al, 2010), we found that average calcium activity 96 correlated positively with expression levels recorded 34 to 42 minutes later for both Arc and c-Fos (Figure 97 1E). The cross-correlation between neural activity and IEG expression levels was increased and relatively 98 stable over a broad range of time lags between neural activity and IEG expression measurement (Figure 99 S1C).…”

supporting

confidence: 88%

Expression of c-Fos and Arc in hippocampal region CA1 marks neurons that exhibit learning-related activity changes

Mahringer

Petersen

Fiser

et al. 2019

Preprint

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Immediate early genes (IEGs) are transcribed in response to neural activity and necessary for many 15 forms of plasticity. However, the dynamics of their expression during learning, as well as their 16 relationship to neural activity, remain unclear. Here we used two-photon imaging in transgenic mice 17 that express a GFP-tagged variant of Arc or c-Fos and a red-shifted calcium indicator to measure 18 learning-related changes in IEG expression levels and neural activity in hippocampal region CA1 as mice 19learned to perform a two-alternative forced choice task. Neural activity levels correlated positively with 20 IEG expression levels in vivo. In addition, we found that with learning, a subset of neurons in CA1 21 increased their responses to the reward-predicting cue, and IEG expression levels early in learning were 22 selectively increased in neurons that would exhibit the strongest learning-related changes. Our findings 23 are consistent with an interpretation of IEG expression levels as markers for experience dependent 24 plasticity. 25 26 to involve increases in the expression of a set of genes, referred to as immediate early genes (IEGs) 33

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supporting

confidence: 88%

Expression of c-Fos and Arc in hippocampal region CA1 marks neurons that exhibit learning-related activity changes

Mahringer

Petersen

Fiser

et al. 2019

Preprint

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“…Consistent with this notion, our estimates of significantly CS-selective cells that emerge with learning fall within the range of the 10-20% of CA1 pyramidal neurons recruited in engrams supporting hippocampal-dependent memory [Tayler et al, 2013, Tanaka et al, 2018, Rao-Ruiz et al, 2019]. If the sparse subset of CS-selective cells we observe do represent engram cells, then this would further support the notion that gating mechanisms exist to ensure sparsity of encoded engrams, since the size of the engram does not vary with behavioral paradigms, such as immobilized, auditory tFC used here compared with contextual learning in freely moving animals [Rao-Ruiz et al, 2019].…”

Section: Discussionsupporting

confidence: 66%

“…These units encode cue information in a learning-dependent manner. It is plausible that these dynamics may relate to descriptions of hippocampal memory “engram cells”, identified via immediate early gene (IEG) products [Liu et al, 2012, Vetere et al, 2017, Tanaka et al, 2018, Rao-Ruiz et al, 2019].…”

Section: Discussionmentioning

confidence: 99%

Hippocampal network reorganization underlies the formation of a temporal association memory

Ahmed

Priestley

Castro

et al. 2019

Preprint

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AbstractEpisodic memory requires linking events in time, a function dependent on the hippocampus. In “trace” fear conditioning, animals learn to associate a neutral cue with an aversive stimulus despite their separation in time by a delay period on the order of tens of seconds. But how this temporal association forms remains unclear. Here we use 2-photon calcium imaging to track neural population dynamics over the complete time-course of learning and show that, in contrast to previous theories, the hippocampus does not generate persistent activity to bridge the time delay. Instead, learning is concomitant with broad changes in the active neural population in CA1. While neural responses were highly stochastic in time, cue identity could be reliably read out from population activity rates over longer timescales after learning. These results question the ubiquity of neural sequences during temporal association learning, and suggest that trace fear conditioning relies on mechanisms that differ from persistent activity accounts of working memory.

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“…Interestingly, all 3 types of place cells displayed a shift towards the descending wave with learning, though this shift was greatest in remapping cells. Recently, a place cell study of engram cells 42 in the mouse hippocampus showed that when engram cells fire bursts of action potentials, they tend to do so on the descending wave of theta 43 , lending support to our findings and suggesting that the remapping cell population may overlap with that of engram cells.…”

Section: Inputs Driving Remappingsupporting

confidence: 86%

Episodic memory encoding by a place cell sub-population

Ormond

Serka

Johansen

2019

Preprint

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Study of the hippocampal place cell system has greatly enhanced our understanding of memory encoding for distinct places, but how episodic memories for distinct experiences occurring within familiar environments are encoded is not clear. One possibility is that different place cell populations encode details of the novel experience or maintain the representation of the unchanged environment. We developed an aversive spatial decision making task which induced partial remapping in CA1, allowing us to identify both remapping and stable cell populations.We found that remapping cells exhibited distinct features not present in stable cells. During memory encoding, their theta phase preferences shifted to earlier phases, when CA3 inputs are strongest. Further, their recruitment into replay events increased during learning, unlike that of stable cells. Our demonstration of a sub-population of place cells identified on the basis of their degree of remapping and exhibiting unique changes in their spike firing properties with learning lend support to a model in which novel and familiar spatial/contextual information is encoded and maintained, respectively, by separate place cell populations.

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The hippocampal engram maps experience but not place

Cited by 193 publications

References 29 publications

Expression of c-Fos and Arc in hippocampal region CA1 marks neurons that exhibit learning-related activity changes

Expression of c-Fos and Arc in hippocampal region CA1 marks neurons that exhibit learning-related activity changes

Hippocampal network reorganization underlies the formation of a temporal association memory

Episodic memory encoding by a place cell sub-population

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