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A hippocampal network for spatial coding during immobility and sleep

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ABSTRACT

How does an animal know where it is when it stops moving? Hippocampal place cells fire at discrete locations as subjects traverse space, thereby providing an explicit neural code for current location during locomotion. In contrast, during awake immobility, the hippocampus is thought to be dominated by neural firing representing past and possible future experience. The question of whether and how the hippocampus constructs a representation of current location in the absence of locomotion has stood unresolved. Here we report that a distinct population of hippocampal neurons, located in the CA2 subregion, signals current location during immobility, and furthermore does so in association with a previously unidentified hippocampus-wide network pattern. In addition, signaling of location persists into brief periods of desynchronization prevalent in slow-wave sleep. The hippocampus thus generates a distinct representation of current location during immobility, pointing to mnemonic processing specific to experience occurring in the absence of locomotion.

No MeSH data available.


Distinct hippocampal neuron population at CA2Diagram of hippocampal recording sites. Recording locations were designated as CA2 sites if found to overlap with the CA2 cytoarchitectural locus24 (dotted lines). CA2 molecular markers are schematized as a yellow band. Additional description is provided in Extended Data Fig. 1. b, Classification of putative principal vs. interneuronal units. Shown is a scatter plot of all hippocampal neural units in the task data set for the three features used to classify units in this study. AC mean: autocorrelation function mean. Open circles: interneuronal (n = 78); plus symbols: principal (n = 991); open diamonds: unclassified (n = 21). c, Firing aligned to SWRs (t = 0: time of SWR onset) in four simultaneously recorded hippocampal putative principal units. Upper sections: SWR-triggered spike rasters (black dots). Grey zones demarcate rest epochs; white zones demarcate task epochs. Lower sections: peri-SWR time histogram (PSTH; 1-ms bins) smoothed with a Gaussian kernel (σ = 10 ms). Red background indicates increased firing during SWRs; blue background indicates lack of increase. The CA2 site units were recorded on the same tetrode. d, Firing aligned to SWRs in four example CA2 N units. Each unit was recorded from a different subject. e, Percentages of P (red) vs. N (blue) units at CA1, CA2, and CA3 recording sites. Numbers correspond to unit counts.
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Figure 11: Distinct hippocampal neuron population at CA2Diagram of hippocampal recording sites. Recording locations were designated as CA2 sites if found to overlap with the CA2 cytoarchitectural locus24 (dotted lines). CA2 molecular markers are schematized as a yellow band. Additional description is provided in Extended Data Fig. 1. b, Classification of putative principal vs. interneuronal units. Shown is a scatter plot of all hippocampal neural units in the task data set for the three features used to classify units in this study. AC mean: autocorrelation function mean. Open circles: interneuronal (n = 78); plus symbols: principal (n = 991); open diamonds: unclassified (n = 21). c, Firing aligned to SWRs (t = 0: time of SWR onset) in four simultaneously recorded hippocampal putative principal units. Upper sections: SWR-triggered spike rasters (black dots). Grey zones demarcate rest epochs; white zones demarcate task epochs. Lower sections: peri-SWR time histogram (PSTH; 1-ms bins) smoothed with a Gaussian kernel (σ = 10 ms). Red background indicates increased firing during SWRs; blue background indicates lack of increase. The CA2 site units were recorded on the same tetrode. d, Firing aligned to SWRs in four example CA2 N units. Each unit was recorded from a different subject. e, Percentages of P (red) vs. N (blue) units at CA1, CA2, and CA3 recording sites. Numbers correspond to unit counts.

Mentions: We recorded neural activity in hippocampal subregions CA1, CA2, CA3, and DG (Fig. 1a) in rats engaged in a hippocampus-dependent spatial memory task21,25, with interleaved rest sessions in an enclosed box. In the task, subjects were trained to alternate between each of three locations (reward wells) in a W-shaped maze (Extended Data Fig. 1a). In examining single neuron (unit) activity, we observed principal units (Fig. 1b) that fired at continuously high rates during immobility (Extended Data Fig. 2a). This basic observation led us to investigate hippocampal activity in this behavioral state.


A hippocampal network for spatial coding during immobility and sleep
Distinct hippocampal neuron population at CA2Diagram of hippocampal recording sites. Recording locations were designated as CA2 sites if found to overlap with the CA2 cytoarchitectural locus24 (dotted lines). CA2 molecular markers are schematized as a yellow band. Additional description is provided in Extended Data Fig. 1. b, Classification of putative principal vs. interneuronal units. Shown is a scatter plot of all hippocampal neural units in the task data set for the three features used to classify units in this study. AC mean: autocorrelation function mean. Open circles: interneuronal (n = 78); plus symbols: principal (n = 991); open diamonds: unclassified (n = 21). c, Firing aligned to SWRs (t = 0: time of SWR onset) in four simultaneously recorded hippocampal putative principal units. Upper sections: SWR-triggered spike rasters (black dots). Grey zones demarcate rest epochs; white zones demarcate task epochs. Lower sections: peri-SWR time histogram (PSTH; 1-ms bins) smoothed with a Gaussian kernel (σ = 10 ms). Red background indicates increased firing during SWRs; blue background indicates lack of increase. The CA2 site units were recorded on the same tetrode. d, Firing aligned to SWRs in four example CA2 N units. Each unit was recorded from a different subject. e, Percentages of P (red) vs. N (blue) units at CA1, CA2, and CA3 recording sites. Numbers correspond to unit counts.
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Figure 11: Distinct hippocampal neuron population at CA2Diagram of hippocampal recording sites. Recording locations were designated as CA2 sites if found to overlap with the CA2 cytoarchitectural locus24 (dotted lines). CA2 molecular markers are schematized as a yellow band. Additional description is provided in Extended Data Fig. 1. b, Classification of putative principal vs. interneuronal units. Shown is a scatter plot of all hippocampal neural units in the task data set for the three features used to classify units in this study. AC mean: autocorrelation function mean. Open circles: interneuronal (n = 78); plus symbols: principal (n = 991); open diamonds: unclassified (n = 21). c, Firing aligned to SWRs (t = 0: time of SWR onset) in four simultaneously recorded hippocampal putative principal units. Upper sections: SWR-triggered spike rasters (black dots). Grey zones demarcate rest epochs; white zones demarcate task epochs. Lower sections: peri-SWR time histogram (PSTH; 1-ms bins) smoothed with a Gaussian kernel (σ = 10 ms). Red background indicates increased firing during SWRs; blue background indicates lack of increase. The CA2 site units were recorded on the same tetrode. d, Firing aligned to SWRs in four example CA2 N units. Each unit was recorded from a different subject. e, Percentages of P (red) vs. N (blue) units at CA1, CA2, and CA3 recording sites. Numbers correspond to unit counts.
Mentions: We recorded neural activity in hippocampal subregions CA1, CA2, CA3, and DG (Fig. 1a) in rats engaged in a hippocampus-dependent spatial memory task21,25, with interleaved rest sessions in an enclosed box. In the task, subjects were trained to alternate between each of three locations (reward wells) in a W-shaped maze (Extended Data Fig. 1a). In examining single neuron (unit) activity, we observed principal units (Fig. 1b) that fired at continuously high rates during immobility (Extended Data Fig. 2a). This basic observation led us to investigate hippocampal activity in this behavioral state.

View Article: PubMed Central - PubMed

ABSTRACT

How does an animal know where it is when it stops moving? Hippocampal place cells fire at discrete locations as subjects traverse space, thereby providing an explicit neural code for current location during locomotion. In contrast, during awake immobility, the hippocampus is thought to be dominated by neural firing representing past and possible future experience. The question of whether and how the hippocampus constructs a representation of current location in the absence of locomotion has stood unresolved. Here we report that a distinct population of hippocampal neurons, located in the CA2 subregion, signals current location during immobility, and furthermore does so in association with a previously unidentified hippocampus-wide network pattern. In addition, signaling of location persists into brief periods of desynchronization prevalent in slow-wave sleep. The hippocampus thus generates a distinct representation of current location during immobility, pointing to mnemonic processing specific to experience occurring in the absence of locomotion.

No MeSH data available.