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A hippocampal network for spatial coding during immobility and sleep

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.


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N wave-coupled CA1 and CA3 principal neuronsExamples of CA1 and CA3 principal units with negative vs. positive STAs during non-SWR immobility. Each column corresponds to data from an individual unit. Upper sections: Non-SWR immobility STA (black trace, ± s.e.m. over individual LFP traces) and RTA (pink trace, ± 2 * s.e.m. over individual LFP traces). Vertical lines correspond to the time of spiking (for STAs) or time of SWRs (for RTAs). The total number of spikes (for STAs) and SWRs (for RTAs) averaged is reported at upper left. The region in which the LFP (at 1-4 Hz) was recorded is indicated at lower right. STAs with amplitudes (measured at the time of spiking) significantly different from 0 μV (p < 0.05, rank-sum) are marked by an asterisk at upper right. The total trace length is 1 s. A horizontal bar centered at the time of spiking indicates 0 μV and corresponds to 200 ms. Scale bars: x: 200 ms, y: 50 μV for STA (black trace); 100 μV for RTA (pink trace). Middle sections: Spatial firing maps. Positions visited by the subject are plotted in grey while positions at which the unit fired are shown as colored opaque points (in green) plotted chronologically and with darker color values at lower speeds. The total number of spikes in the epoch is reported at upper right. Shown is the 15-minute task epoch in which the unit had the highest mean firing rate. Spikes during SWRs are omitted from all plots. Lower sections: Well firing rasters. The time of well entry (t = 0) is plotted as a grey line. SWR periods are plotted in the background as pink zones.
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Figure 9: N wave-coupled CA1 and CA3 principal neuronsExamples of CA1 and CA3 principal units with negative vs. positive STAs during non-SWR immobility. Each column corresponds to data from an individual unit. Upper sections: Non-SWR immobility STA (black trace, ± s.e.m. over individual LFP traces) and RTA (pink trace, ± 2 * s.e.m. over individual LFP traces). Vertical lines correspond to the time of spiking (for STAs) or time of SWRs (for RTAs). The total number of spikes (for STAs) and SWRs (for RTAs) averaged is reported at upper left. The region in which the LFP (at 1-4 Hz) was recorded is indicated at lower right. STAs with amplitudes (measured at the time of spiking) significantly different from 0 μV (p < 0.05, rank-sum) are marked by an asterisk at upper right. The total trace length is 1 s. A horizontal bar centered at the time of spiking indicates 0 μV and corresponds to 200 ms. Scale bars: x: 200 ms, y: 50 μV for STA (black trace); 100 μV for RTA (pink trace). Middle sections: Spatial firing maps. Positions visited by the subject are plotted in grey while positions at which the unit fired are shown as colored opaque points (in green) plotted chronologically and with darker color values at lower speeds. The total number of spikes in the epoch is reported at upper right. Shown is the 15-minute task epoch in which the unit had the highest mean firing rate. Spikes during SWRs are omitted from all plots. Lower sections: Well firing rasters. The time of well entry (t = 0) is plotted as a grey line. SWR periods are plotted in the background as pink zones.

Mentions: We then asked whether neurons outside of CA2 were also N wave-coupled. We identified N wave-coupled units in CA1, CA3, and DG (Fig. 4e-i, Extended Data Figs. 7d-g, 8, 9), indicating that the N wave reflects a hippocampus-wide network pattern. Critically, a distinct subset of principal units was N wave-coupled (CA1: 50 units, CA3: 34 units, Fig. 4g-i, Extended Data Figs. 8, 9). As with CA2 N units, these units fired more during immobility than during movement (Extended Data Fig. 8b) and showed unequivocal location-specific firing during immobility (Fig. 4g, i and Extended Data Figs. 8d, e, 9), thereby linking the N wave network pattern to spatial coding during immobility across the hippocampus.


A hippocampal network for spatial coding during immobility and sleep
N wave-coupled CA1 and CA3 principal neuronsExamples of CA1 and CA3 principal units with negative vs. positive STAs during non-SWR immobility. Each column corresponds to data from an individual unit. Upper sections: Non-SWR immobility STA (black trace, ± s.e.m. over individual LFP traces) and RTA (pink trace, ± 2 * s.e.m. over individual LFP traces). Vertical lines correspond to the time of spiking (for STAs) or time of SWRs (for RTAs). The total number of spikes (for STAs) and SWRs (for RTAs) averaged is reported at upper left. The region in which the LFP (at 1-4 Hz) was recorded is indicated at lower right. STAs with amplitudes (measured at the time of spiking) significantly different from 0 μV (p < 0.05, rank-sum) are marked by an asterisk at upper right. The total trace length is 1 s. A horizontal bar centered at the time of spiking indicates 0 μV and corresponds to 200 ms. Scale bars: x: 200 ms, y: 50 μV for STA (black trace); 100 μV for RTA (pink trace). Middle sections: Spatial firing maps. Positions visited by the subject are plotted in grey while positions at which the unit fired are shown as colored opaque points (in green) plotted chronologically and with darker color values at lower speeds. The total number of spikes in the epoch is reported at upper right. Shown is the 15-minute task epoch in which the unit had the highest mean firing rate. Spikes during SWRs are omitted from all plots. Lower sections: Well firing rasters. The time of well entry (t = 0) is plotted as a grey line. SWR periods are plotted in the background as pink zones.
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Figure 9: N wave-coupled CA1 and CA3 principal neuronsExamples of CA1 and CA3 principal units with negative vs. positive STAs during non-SWR immobility. Each column corresponds to data from an individual unit. Upper sections: Non-SWR immobility STA (black trace, ± s.e.m. over individual LFP traces) and RTA (pink trace, ± 2 * s.e.m. over individual LFP traces). Vertical lines correspond to the time of spiking (for STAs) or time of SWRs (for RTAs). The total number of spikes (for STAs) and SWRs (for RTAs) averaged is reported at upper left. The region in which the LFP (at 1-4 Hz) was recorded is indicated at lower right. STAs with amplitudes (measured at the time of spiking) significantly different from 0 μV (p < 0.05, rank-sum) are marked by an asterisk at upper right. The total trace length is 1 s. A horizontal bar centered at the time of spiking indicates 0 μV and corresponds to 200 ms. Scale bars: x: 200 ms, y: 50 μV for STA (black trace); 100 μV for RTA (pink trace). Middle sections: Spatial firing maps. Positions visited by the subject are plotted in grey while positions at which the unit fired are shown as colored opaque points (in green) plotted chronologically and with darker color values at lower speeds. The total number of spikes in the epoch is reported at upper right. Shown is the 15-minute task epoch in which the unit had the highest mean firing rate. Spikes during SWRs are omitted from all plots. Lower sections: Well firing rasters. The time of well entry (t = 0) is plotted as a grey line. SWR periods are plotted in the background as pink zones.
Mentions: We then asked whether neurons outside of CA2 were also N wave-coupled. We identified N wave-coupled units in CA1, CA3, and DG (Fig. 4e-i, Extended Data Figs. 7d-g, 8, 9), indicating that the N wave reflects a hippocampus-wide network pattern. Critically, a distinct subset of principal units was N wave-coupled (CA1: 50 units, CA3: 34 units, Fig. 4g-i, Extended Data Figs. 8, 9). As with CA2 N units, these units fired more during immobility than during movement (Extended Data Fig. 8b) and showed unequivocal location-specific firing during immobility (Fig. 4g, i and Extended Data Figs. 8d, e, 9), thereby linking the N wave network pattern to spatial coding during immobility across the hippocampus.

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.


Related in: MedlinePlus