Neural Population-Level Memory Traces in the Mouse Hippocampus
Publication Date
December 16, 2009
Journal
PLOS ONE
Authors
Guifen Chen, L. Phillip Wang & Joe Z. Tsien
Volume
4
Issue
12
Pages
e8256
DOI
https://dx.plos.org/10.1371/journal.pone.0008256
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0008256
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/20016843
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2788416
Europe PMC
http://europepmc.org/abstract/MED/20016843
Web of Science
000272834000007
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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/432644", "https://ndownloader.figshare.com/files/432654", "https://ndownloader.figshare.com/files/432691", "https://ndownloader.figshare.com/files/432753", "https://ndownloader.figshare.com/files/432827", "https://ndownloader.figshare.com/files/432867", "https://ndownloader.figshare.com/files/432902", "https://ndownloader.figshare.com/files/432949", "https://ndownloader.figshare.com/files/433003", "https://ndownloader.figshare.com/files/433041", "https://ndownloader.figshare.com/files/433090"], "description"=>"<div><p>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.</p></div>", "links"=>[], "tags"=>["neural", "population-level", "traces", "hippocampus"], "article_id"=>145370, "categories"=>["Neuroscience"], "users"=>["Guifen Chen", "L. Phillip Wang", "Joe Z. Tsien"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0008256.s001", "https://dx.doi.org/10.1371/journal.pone.0008256.s002", "https://dx.doi.org/10.1371/journal.pone.0008256.s003", "https://dx.doi.org/10.1371/journal.pone.0008256.s004", "https://dx.doi.org/10.1371/journal.pone.0008256.s005", "https://dx.doi.org/10.1371/journal.pone.0008256.s006", "https://dx.doi.org/10.1371/journal.pone.0008256.s007", "https://dx.doi.org/10.1371/journal.pone.0008256.s008", "https://dx.doi.org/10.1371/journal.pone.0008256.s009", "https://dx.doi.org/10.1371/journal.pone.0008256.s010", "https://dx.doi.org/10.1371/journal.pone.0008256.s011"], "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Neural_Population_Level_Memory_Traces_in_the_Mouse_Hippocampus/145370", "title"=>"Neural Population-Level Memory Traces in the Mouse Hippocampus", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-12-16 01:29:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/871620"], "description"=>"<p>(<b>A</b>) The top panel shows the spectrogram of local field potentials during a 60-sec epoch of trace recall in mouse #1. The blue bar on the top indicates the non-freezing state, whereas the red bar indicates the freezing state of the animal. The time scale is matched with the spike raster shown below. Colored triangles at the bottom indicate the various moments at which encoding patterns were retrieved. To initiate the trace memory recall, a 2-sec tone was played. (<b>B</b>) Global MDA analysis shows that the data from the recall chamber and the conditioning chamber formed a single tone-pattern ellipsoid. The conditioned tone patterns (see the rectangle in the left panel) were recomputed by a second-step MDA to achieve finer separation for the difference of contextual environments. The purple trajectory is the recall-triggered CS pattern at the time when the tone was played, indicated by the purple triangle with a starred B in (A). (<b>C</b>) Type-I trajectory (purple) was retrieved during the first 1-min trace recall trial. This trajectory occurred at 53.5 seconds, indicated by the purple triangle with a starred C in (A). (<b>D</b>) Type-II trajectory (pink) was retrieved during trace recall. This trajectory occurred at 28.2 seconds, indicated by the pink triangle with a starred D in (A). (<b>E</b>) Additional types of ensemble trajectories were also detected during the trace recall trials. In particular, the dark green trajectory seemed to visit both the tone-at-recall cluster and the tone-at-training cluster. Whereas the light green trajectory visited the subspace between the tone-at-training cluster and the US cluster. (<b>F</b>) The averaged percentages of different types of ensemble patterns retrieved during the trace recall sessions from six recorded mice.</p>", "links"=>[], "tags"=>["patterns"], "article_id"=>542087, "categories"=>["Neuroscience"], "users"=>["Guifen Chen", "L. Phillip Wang", "Joe Z. Tsien"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008256.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ensemble_dynamic_patterns_during_the_trace_recall_test_/542087", "title"=>"Ensemble dynamic patterns during the trace recall test.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-16 00:34:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/871754"], "description"=>"<p>(<b>A</b>) Representative ensemble tone traces during trace recall (Left panel). The right panel shows the time distribution of the averaged occurrences of this type of trajectories over seven recall-trials in mouse #1. Time zero indicates the moment when the recall tone was delivered. The numbers of trajectories were pooled every 5 seconds. (<b>B</b>) Representative ensemble shock traces during the traced memory recall session are shown (Left panel). The right panel shows the time distribution of the averaged occurrences of this type of trajectories over seven recall-trials in the same mouse. The same analysis reveals a salient peak in the occurrences of the US trajectories around the traced interval time point. Time zero indicates the onset moment when the recall tone was delivered. The tone lasted 2 seconds, thus the absolute amount of time between the offset of the tone and the retrieval peak was around 20 seconds. (<b>C</b>) The peaked occurrences of the US ensemble trajectories were observed in five out of the six recorded mice. Each colored plot represents a mouse. (<b>D</b>) The color matrix shows the retrievals of the US ensemble traces in six individual mice around the traced interval time (20±2.5 sec after the offset of the recall tone) at each of the seven trials. Yellow squares represent the occurrences of the correct US ensemble patterns, whereas blue squares indicate the absence of US patterns at the time point of this trace interval. (<b>E</b>) The exact time distribution of the 31 correct US pattern retrievals around the traced interval time in all six mice. Please note that the 22-sec time point is from the onset of the recall tone (which lasts 2 seconds). (<b>F</b>) Lack of distinct peak in the traced fear freezing over the 1-min recall trials. Blue triangles show the five-second averaged freezing responses over seven recall-trials (1-min per trial) from six recorded mice. Red stars show the US pattern retrieval distribution. Correlation between the averaged freezing response and occurrences of US traces was still significant (r = 0.5851, p<0.05), despite the absence of a distinct peak in freezing.</p>", "links"=>[], "tags"=>["peaked", "re-appearance", "patterns", "traced", "indicates"], "article_id"=>542211, "categories"=>["Neuroscience"], "users"=>["Guifen Chen", "L. Phillip Wang", "Joe Z. Tsien"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008256.g006", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_peaked_re_appearance_of_the_US_patterns_at_the_traced_time_interval_indicates_the_memory_of_time_/542211", "title"=>"The peaked re-appearance of the US patterns at the traced time interval indicates the memory of time.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-16 00:36:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/871328"], "description"=>"<p>(<b>A</b>) Spectrogram of local field potentials during the third CS-US pairing training. The blue color bar on the top indicates the non-freezing state, whereas the red bar indicates the freezing state of the animal. The color scale represents spectral power. The time scale is matched with the spike raster shown below. (<b>B</b>) Three post-stimulus immediate reactivations of the ensemble encoding patterns during the third learning trial were detected, marked by small triangles at the bottom of the spike raster. The sixty-sec spike-raster plot from mouse #1 is the same as the one shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0008256#pone-0008256-g002\" target=\"_blank\">Fig. 2D</a>. (<b>C</b>) An immediate reactivation, shown by the blue trajectory, was detected at the moment marked by the blue triangle at the bottom of (B). Similar to its original encoding pattern (shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0008256#pone-0008256-g002\" target=\"_blank\">Fig. 2E</a>), this reactivation trajectory transiently visited the CS cluster. This CS Trace (type-I) lasted about 0.8 seconds. (<b>D</b>) A second reactivation, shown by the pink trajectory, occurred at ∼9 sec shown by the pink triangle in (B). This trajectory visited the US cluster. This US Trace (Type-II) lasted about 0.7 seconds. (<b>E</b>) A third reactivation (red trajectory) took place at 43 sec, indicated by the red triangle in (B). This 1-sec association trajectory (Type-III), just like the encoding traces shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0008256#pone-0008256-g002\" target=\"_blank\">Fig. 2F</a>, first visited the US cluster and then toward the CS cluster before returning to the Rest. The same directionality was maintained. (<b>F</b>) Averaged numbers of reactivations (all three major types of traces) in six recorded mice over seven learning trials. The blue open triangles presents the averaged reactivation numbers within the 20-sec interval of the same CS-US pairing, whereas the red open triangles show the averaged reactivation numbers within the 60-sec after the paired US was delivered. The linear regression lines suggest the accumulative effects of pairings on the ensemble trace formation. (<b>G</b>) Numbers of immediate reactivations and the amounts of immediate freezing over seven trials in mouse #1. Cross-correlation analysis shows the correlation between freezing responses and occurrence numbers of reactivations was highly significant (r = 0.9657, p<0.001). Averaged freezing responses and the total numbers of reactivations were calculated from the period between the tone offset and the 60-sec after US presentation. (<b>H</b>) Averaged immediate freezing responses and the total numbers of reactivations were calculated from six mice. The correlation between freezing and reactivations was again highly significant (r = 0.9551, p<0.001).</p>", "links"=>[], "tags"=>["ensemble", "patterns"], "article_id"=>541788, "categories"=>["Neuroscience"], "users"=>["Guifen Chen", "L. Phillip Wang", "Joe Z. Tsien"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008256.g003", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reactivations_of_ensemble_dynamic_patterns_during_learning_/541788", "title"=>"Reactivations of ensemble dynamic patterns during learning.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-16 00:29:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/871005"], "description"=>"<p>(<b>A</b>) Illustration of a fear conditioning chamber for producing a tone-shock trace fear memory. A neutral tone precedes a mild foot-shock via a metal grid floor. (<b>B</b>) The trace interval between the offset of the tone (2 sec) and the onset of the foot shock (0.3 sec) is 20 seconds. (<b>C</b>) Schematic representation of experimental paradigm for trace fear conditioning. On the training day, the experiment begins as follows: one-hour pre-training sleep/rest in home cage; pre-training exploration in the conditioning chamber; trace conditioning in the conditioning chamber; one-hour post-training rest/sleep in home cage; contextual recall in the conditioning chamber; trace conditioning recall in a novel chamber. (<b>D</b>) Immediate freezing in mouse #1 increased as the CS-US pairing repeated during the training phase. (<b>E</b>) Contextual freezing in the 1-h contextual retention test suggests the contextual fear formation in mouse #1; at the end of the 5-min test, freezing decreased as there was no reinforcement shock. (<b>F</b>) Robust trace freezing upon the recall tone. The tone was presented for seven times (trials) with a 1-min interval. (<b>G</b>) As a group (n = 10), there was a significant contextual freezing as revealed by the 1-h contextual retention test (62.5%±5.5%, p<0.001). (<b>H</b>) The same set of mice showed a significant increased freezing during the 1-h trace retention test (n = 10, 61.5%±5.3%, p<0.001).</p>", "links"=>[], "tags"=>["neuroscience/animal cognition", "neuroscience/behavioral neuroscience", "neuroscience/cognitive neuroscience"], "article_id"=>541465, "categories"=>["Neuroscience"], "users"=>["Guifen Chen", "L. Phillip Wang", "Joe Z. Tsien"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008256.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Associative_trace_fear_conditioning_/541465", "title"=>"Associative trace fear conditioning.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-16 00:24:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/871165"], "description"=>"<p>(<b>A</b>) Sixty-sec spike rasters of a selective set of CA1 units during the first CS-US pairing (105 units shown out of 208 simultaneously recorded units from mouse #1 for demonstration). The different colors represent several groups of cells with different response properties. The units listed at the bottom were selected from the non-responsive group (see details in SF 4). (<b>B</b>) MDA analysis shows ensemble patterns and dynamic trajectories in response to the first CS before the US arrived. The grey, blue and red ellipsoids represent the resting state, tone, and foot-shock clusters, respectively. The grey trajectory shows a transient (∼1-sec) ensemble dynamics at the moment marked by the arrow B near the zero time point in (A) in response to the first tone before the paired US arrived. This trajectory remained largely within the rest cluster, indicating that CA1 did not respond to the neutral tone initially. (<b>C</b>) A robust dynamic trajectory moving from the Rest cluster to Shock cluster was detected when the first paired US was delivered at the time point marked by the arrow C in (A). This transient trace lasted about 1.5 seconds. (<b>D</b>) The sixty-sec spike rasters demonstrate neural activity of the same set of cells shown in (A) during the third CS/US pairing. (<b>E</b>) The CS presentation in this third trial elicited a robust pattern (blue trajectory). The duration corresponds to the blue bar length in (D) marked by the arrow E. (<b>F</b>) The third paired US triggered an associative trajectory that transversed the shock cluster and the conditioned tone cluster. The color-coded trajectory, spanning for about 3 seconds, corresponds to the moment indicated by the colored bar in (D). (<b>G</b>) Two more examples of the unique US-CS associative trajectories elicited by foot shock at the fourth and sixth trials in the same animal (mouse #1) are shown here. The arrows indicate the moving directions of the ensemble trajectories. (<b>H</b>) The six-by-seven color matrix shows the occurrences of US-CS association patterns over seven trials from the six recorded mice. The blue squares indicate that foot shock (US) only triggered US ensemble trajectories early on, whereas the yellow squares indicate the US-CS association trajectory was elicited by foot shock, which became more prevalent after pairings.</p>", "links"=>[], "tags"=>["patterns"], "article_id"=>541631, "categories"=>["Neuroscience"], "users"=>["Guifen Chen", "L. Phillip Wang", "Joe Z. Tsien"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008256.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ensemble_dynamic_patterns_during_learning_/541631", "title"=>"Ensemble dynamic patterns during learning.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-16 00:27:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/871459"], "description"=>"<p>(<b>A</b>) The top panel shows the spectrogram of local field potentials during the 60-sec epoch of the contextual recall test in mouse #1. The blue bar on the top indicates the non-freezing state, whereas the red bar indicates the freezing state of the animal. The color scale represents spectral power. The time scale is matched with the spike raster shown below. The colored triangles at the bottom indicate the moments at which encoding patterns re-appeared. (<b>B</b>) The blue trajectory shows that a representative CS trace (Type I) was retrieved, indicated by the star marked with B at the bottom of the raster in (A). This transient dynamic lasted about one second. (<b>C</b>) The pink trajectory shows a representative US trace that lasts about 0.7 seconds (marked by the pink triangle with C in (A), Type II). (<b>D</b>) The red trajectory is a representative US-CS association trace (the red triangle with D in (A), Type III). This trajectory occurred for about 0.8 seconds. (<b>E</b>) The green trace shows a type of different traces often seen during recall test. It visited the space between the US and CS clusters and lasted about one second. (<b>F</b>) The colored trajectory shows a Type III trace that was retrieved at the time indicated by the red triangle with F in (A). This trajectory occurred in the non-freezing state, and interestingly, had a reversed directionality, namely, moving from the CS ellipsoid to the US ellipsoid. It lasted about three seconds. (<b>G</b>) The percentages of different types of ensemble patterns during contextual recall in six mice. (<b>H</b>) Freezing responses and the total numbers of pattern retrievals were calculated and compared during the entire 5-min contextual recall test (mouse #1). The blue circles are the freezing responses counted in every 30 seconds; the red circles show the averaged numbers of three major types of ensemble traces counted in the same 30 seconds. Cross-correlation analysis shows that the correlation between freezing responses and occurrences of pattern retrievals was significant (r = 0.8840, p<0.001). (<b>I</b>) Averaged freezing responses in six mice are also tightly correlated with their averaged numbers of total pattern retrievals during the contextual recall tests (r = 0.8956, p<0.05). Each circle represents the data from a single mouse. This between-animals plot indicates that the numbers of pattern retrieved is almost in linear proportion to behavioral performances as measured by the amounts of contextual freezing. The animal which had a fewer number of pattern retrieved also showed lower fear memory freezing, whereas the mice which had high numbers of pattern recalled exhibited highest amount of freezing.</p>", "links"=>[], "tags"=>["patterns", "contextual"], "article_id"=>541919, "categories"=>["Neuroscience"], "users"=>["Guifen Chen", "L. Phillip Wang", "Joe Z. Tsien"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008256.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ensemble_dynamic_patterns_during_contextual_recall_/541919", "title"=>"Ensemble dynamic patterns during contextual recall.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-16 00:31:59"}

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  • {"unique-ip"=>"12", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
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  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"14", "full-text"=>"19", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
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  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"14", "full-text"=>"7", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"20", "full-text"=>"9", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"11", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"27", "full-text"=>"21", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"13", "full-text"=>"15", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}

Relative Metric

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