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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.


Related in: MedlinePlus

A novel hippocampal network pattern marks spatial coding during immobilitySchematic of recording configuration. SWRs (pink symbol) were detected with CA1 site electrodes, while wide-band LFP was taken from CA2, CA3, and DG site electrodes. Blue and red symbols refer to CA2 N and CA2 P units, respectively, analyzed in b-d. b, Example CA2 N (blue symbol, first column) and CA2 P (red symbol, second column) unit spike-triggered average (STA) and SWR-triggered average (RTA; pink symbol, third column) of hippocampal CA2, CA3, and DG LFP from non-SWR immobility periods. Vertical lines indicate the time of spiking (STA) or time of SWR (RTA). The two units were recorded simultaneously and on the same tetrode. SWRs averaged in the RTA were detected in the same recording epochs as the units. The total number of events averaged is reported at upper right. Trace width indicates ± s.e.m. over single LFP traces. Trace length: 2 s. Scale bars: x: 250 ms, y: 100 μV. c, Mean STAs for CA2 N and CA2 P unit populations for non-SWR immobility periods. The mean RTA was calculated from single RTAs matching the recording epochs of N unit STAs, and thus have the same sample size. Trace width indicates ± s.e.m. over unit STAs/RTAs. Trace length: 2 s. Scale bars: x: 250 ms, y: 100 μV. d, Power spectral density (PSD) of STAs and RTAs of DG LFP. The mean PSD is plotted as a black line, with ± s.e.m. over single averages plotted in grey (locomotor periods: CA2 N, n = 39 units; CA2 P, n = 85; non-SWR immobility periods: CA2 N, n = 47; CA2 P, n = 72; RTAs matched to CA2 N units: n = 47). e, Schematic of additional hippocampal neurons analyzed with STAs. Interneuronal units (left, grey circles) recorded in the principal cell layers of CA1, CA2, CA3 and DG analyzed in f and Extended Data Fig. 7d-g. Principal units (right, grey triangles) recorded in CA1 and CA3 analyzed in g-i and Extended Data Figs. 8 and 9. STAs in f-i were taken for 1-4 Hz LFP, analyzing spikes from non-SWR immobility periods. f, N wave firing in four example interneuronal units. Plotted are unit STAs and RTAs. Trace width indicates ± s.e.m. (STA) or ± 2 s.e.m. (RTA) over single LFP traces. Vertical line: time of spiking (STAs) or SWRs (RTAs). The hippocampal region in which the unit was recorded is reported at upper right. The number of spikes or SWRs averaged is indicated at upper and lower left, respectively. Trace length: 1 s. Horizontal line (200 ms in length): 0 μV. DG LFP was used in each example except for the CA3 unit, which used CA3 LFP. Scale bars: x: 200 ms, y: 50 μV for STA (black), 100 μV for RTA (pink). g, N wave firing and well specificity in four example CA1/CA3 principal units. Top: unit STAs and RTAs, following the plotting conventions in f. DG LFP was used in each example. Bottom: well firing rasters correspondent with each unit. Grey line: time of well entry (t = 0). SWR periods plotted as pink zones. h, CA1 and CA3 unit STAs. Color indicates voltage. For each unit, LFP (1-4 Hz) from DG, CA3, or CA2 (in decreasing order of preference) was used. Unit STAs were grouped by polarity at the time of spiking (t = 0) and sorted by the time of the local extremum (peak for positive; trough for negative) nearest the time of spiking. Units with positive voltage peaks at the time of spiking were classified as N wave-coupled. i, Well specificity distributions for CA1 and CA3 principal unit populations classified by STA. For both CA1 and CA3 populations, units with positive STAs (N wave-coupled) showed higher well specificity than units with negative STAs (mean ± s.e.m.; CA1 pos.: 0.85 ± 0.03; CA1 neg.: 0.65 ± 0.04, CA1 pos. vs. CA1 neg., p < 10-5, rank-sum; CA3 pos.: 0.77 ± 0.04; CA3 neg.: 0.53 ± 0.04, CA3 pos. vs. CA3 neg., p < 0.001, rank-sum).
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Figure 14: A novel hippocampal network pattern marks spatial coding during immobilitySchematic of recording configuration. SWRs (pink symbol) were detected with CA1 site electrodes, while wide-band LFP was taken from CA2, CA3, and DG site electrodes. Blue and red symbols refer to CA2 N and CA2 P units, respectively, analyzed in b-d. b, Example CA2 N (blue symbol, first column) and CA2 P (red symbol, second column) unit spike-triggered average (STA) and SWR-triggered average (RTA; pink symbol, third column) of hippocampal CA2, CA3, and DG LFP from non-SWR immobility periods. Vertical lines indicate the time of spiking (STA) or time of SWR (RTA). The two units were recorded simultaneously and on the same tetrode. SWRs averaged in the RTA were detected in the same recording epochs as the units. The total number of events averaged is reported at upper right. Trace width indicates ± s.e.m. over single LFP traces. Trace length: 2 s. Scale bars: x: 250 ms, y: 100 μV. c, Mean STAs for CA2 N and CA2 P unit populations for non-SWR immobility periods. The mean RTA was calculated from single RTAs matching the recording epochs of N unit STAs, and thus have the same sample size. Trace width indicates ± s.e.m. over unit STAs/RTAs. Trace length: 2 s. Scale bars: x: 250 ms, y: 100 μV. d, Power spectral density (PSD) of STAs and RTAs of DG LFP. The mean PSD is plotted as a black line, with ± s.e.m. over single averages plotted in grey (locomotor periods: CA2 N, n = 39 units; CA2 P, n = 85; non-SWR immobility periods: CA2 N, n = 47; CA2 P, n = 72; RTAs matched to CA2 N units: n = 47). e, Schematic of additional hippocampal neurons analyzed with STAs. Interneuronal units (left, grey circles) recorded in the principal cell layers of CA1, CA2, CA3 and DG analyzed in f and Extended Data Fig. 7d-g. Principal units (right, grey triangles) recorded in CA1 and CA3 analyzed in g-i and Extended Data Figs. 8 and 9. STAs in f-i were taken for 1-4 Hz LFP, analyzing spikes from non-SWR immobility periods. f, N wave firing in four example interneuronal units. Plotted are unit STAs and RTAs. Trace width indicates ± s.e.m. (STA) or ± 2 s.e.m. (RTA) over single LFP traces. Vertical line: time of spiking (STAs) or SWRs (RTAs). The hippocampal region in which the unit was recorded is reported at upper right. The number of spikes or SWRs averaged is indicated at upper and lower left, respectively. Trace length: 1 s. Horizontal line (200 ms in length): 0 μV. DG LFP was used in each example except for the CA3 unit, which used CA3 LFP. Scale bars: x: 200 ms, y: 50 μV for STA (black), 100 μV for RTA (pink). g, N wave firing and well specificity in four example CA1/CA3 principal units. Top: unit STAs and RTAs, following the plotting conventions in f. DG LFP was used in each example. Bottom: well firing rasters correspondent with each unit. Grey line: time of well entry (t = 0). SWR periods plotted as pink zones. h, CA1 and CA3 unit STAs. Color indicates voltage. For each unit, LFP (1-4 Hz) from DG, CA3, or CA2 (in decreasing order of preference) was used. Unit STAs were grouped by polarity at the time of spiking (t = 0) and sorted by the time of the local extremum (peak for positive; trough for negative) nearest the time of spiking. Units with positive voltage peaks at the time of spiking were classified as N wave-coupled. i, Well specificity distributions for CA1 and CA3 principal unit populations classified by STA. For both CA1 and CA3 populations, units with positive STAs (N wave-coupled) showed higher well specificity than units with negative STAs (mean ± s.e.m.; CA1 pos.: 0.85 ± 0.03; CA1 neg.: 0.65 ± 0.04, CA1 pos. vs. CA1 neg., p < 10-5, rank-sum; CA3 pos.: 0.77 ± 0.04; CA3 neg.: 0.53 ± 0.04, CA3 pos. vs. CA3 neg., p < 0.001, rank-sum).

Mentions: We were struck by the fact that the firing pattern of N units was not only unorthodox (Fig. 1) but also had unambiguous behavioral (Fig. 2) and representational (Fig. 3) correlates. We hypothesized that this distinctive firing was the result of an unidentified input pattern in the hippocampus. To evaluate this possibility, we calculated CA2 site (N and P) unit spike-triggered averages (STAs) of hippocampal local field potential (LFP)18, analyzing locomotor and immobility periods separately (Fig. 4a).


A hippocampal network for spatial coding during immobility and sleep
A novel hippocampal network pattern marks spatial coding during immobilitySchematic of recording configuration. SWRs (pink symbol) were detected with CA1 site electrodes, while wide-band LFP was taken from CA2, CA3, and DG site electrodes. Blue and red symbols refer to CA2 N and CA2 P units, respectively, analyzed in b-d. b, Example CA2 N (blue symbol, first column) and CA2 P (red symbol, second column) unit spike-triggered average (STA) and SWR-triggered average (RTA; pink symbol, third column) of hippocampal CA2, CA3, and DG LFP from non-SWR immobility periods. Vertical lines indicate the time of spiking (STA) or time of SWR (RTA). The two units were recorded simultaneously and on the same tetrode. SWRs averaged in the RTA were detected in the same recording epochs as the units. The total number of events averaged is reported at upper right. Trace width indicates ± s.e.m. over single LFP traces. Trace length: 2 s. Scale bars: x: 250 ms, y: 100 μV. c, Mean STAs for CA2 N and CA2 P unit populations for non-SWR immobility periods. The mean RTA was calculated from single RTAs matching the recording epochs of N unit STAs, and thus have the same sample size. Trace width indicates ± s.e.m. over unit STAs/RTAs. Trace length: 2 s. Scale bars: x: 250 ms, y: 100 μV. d, Power spectral density (PSD) of STAs and RTAs of DG LFP. The mean PSD is plotted as a black line, with ± s.e.m. over single averages plotted in grey (locomotor periods: CA2 N, n = 39 units; CA2 P, n = 85; non-SWR immobility periods: CA2 N, n = 47; CA2 P, n = 72; RTAs matched to CA2 N units: n = 47). e, Schematic of additional hippocampal neurons analyzed with STAs. Interneuronal units (left, grey circles) recorded in the principal cell layers of CA1, CA2, CA3 and DG analyzed in f and Extended Data Fig. 7d-g. Principal units (right, grey triangles) recorded in CA1 and CA3 analyzed in g-i and Extended Data Figs. 8 and 9. STAs in f-i were taken for 1-4 Hz LFP, analyzing spikes from non-SWR immobility periods. f, N wave firing in four example interneuronal units. Plotted are unit STAs and RTAs. Trace width indicates ± s.e.m. (STA) or ± 2 s.e.m. (RTA) over single LFP traces. Vertical line: time of spiking (STAs) or SWRs (RTAs). The hippocampal region in which the unit was recorded is reported at upper right. The number of spikes or SWRs averaged is indicated at upper and lower left, respectively. Trace length: 1 s. Horizontal line (200 ms in length): 0 μV. DG LFP was used in each example except for the CA3 unit, which used CA3 LFP. Scale bars: x: 200 ms, y: 50 μV for STA (black), 100 μV for RTA (pink). g, N wave firing and well specificity in four example CA1/CA3 principal units. Top: unit STAs and RTAs, following the plotting conventions in f. DG LFP was used in each example. Bottom: well firing rasters correspondent with each unit. Grey line: time of well entry (t = 0). SWR periods plotted as pink zones. h, CA1 and CA3 unit STAs. Color indicates voltage. For each unit, LFP (1-4 Hz) from DG, CA3, or CA2 (in decreasing order of preference) was used. Unit STAs were grouped by polarity at the time of spiking (t = 0) and sorted by the time of the local extremum (peak for positive; trough for negative) nearest the time of spiking. Units with positive voltage peaks at the time of spiking were classified as N wave-coupled. i, Well specificity distributions for CA1 and CA3 principal unit populations classified by STA. For both CA1 and CA3 populations, units with positive STAs (N wave-coupled) showed higher well specificity than units with negative STAs (mean ± s.e.m.; CA1 pos.: 0.85 ± 0.03; CA1 neg.: 0.65 ± 0.04, CA1 pos. vs. CA1 neg., p < 10-5, rank-sum; CA3 pos.: 0.77 ± 0.04; CA3 neg.: 0.53 ± 0.04, CA3 pos. vs. CA3 neg., p < 0.001, rank-sum).
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Figure 14: A novel hippocampal network pattern marks spatial coding during immobilitySchematic of recording configuration. SWRs (pink symbol) were detected with CA1 site electrodes, while wide-band LFP was taken from CA2, CA3, and DG site electrodes. Blue and red symbols refer to CA2 N and CA2 P units, respectively, analyzed in b-d. b, Example CA2 N (blue symbol, first column) and CA2 P (red symbol, second column) unit spike-triggered average (STA) and SWR-triggered average (RTA; pink symbol, third column) of hippocampal CA2, CA3, and DG LFP from non-SWR immobility periods. Vertical lines indicate the time of spiking (STA) or time of SWR (RTA). The two units were recorded simultaneously and on the same tetrode. SWRs averaged in the RTA were detected in the same recording epochs as the units. The total number of events averaged is reported at upper right. Trace width indicates ± s.e.m. over single LFP traces. Trace length: 2 s. Scale bars: x: 250 ms, y: 100 μV. c, Mean STAs for CA2 N and CA2 P unit populations for non-SWR immobility periods. The mean RTA was calculated from single RTAs matching the recording epochs of N unit STAs, and thus have the same sample size. Trace width indicates ± s.e.m. over unit STAs/RTAs. Trace length: 2 s. Scale bars: x: 250 ms, y: 100 μV. d, Power spectral density (PSD) of STAs and RTAs of DG LFP. The mean PSD is plotted as a black line, with ± s.e.m. over single averages plotted in grey (locomotor periods: CA2 N, n = 39 units; CA2 P, n = 85; non-SWR immobility periods: CA2 N, n = 47; CA2 P, n = 72; RTAs matched to CA2 N units: n = 47). e, Schematic of additional hippocampal neurons analyzed with STAs. Interneuronal units (left, grey circles) recorded in the principal cell layers of CA1, CA2, CA3 and DG analyzed in f and Extended Data Fig. 7d-g. Principal units (right, grey triangles) recorded in CA1 and CA3 analyzed in g-i and Extended Data Figs. 8 and 9. STAs in f-i were taken for 1-4 Hz LFP, analyzing spikes from non-SWR immobility periods. f, N wave firing in four example interneuronal units. Plotted are unit STAs and RTAs. Trace width indicates ± s.e.m. (STA) or ± 2 s.e.m. (RTA) over single LFP traces. Vertical line: time of spiking (STAs) or SWRs (RTAs). The hippocampal region in which the unit was recorded is reported at upper right. The number of spikes or SWRs averaged is indicated at upper and lower left, respectively. Trace length: 1 s. Horizontal line (200 ms in length): 0 μV. DG LFP was used in each example except for the CA3 unit, which used CA3 LFP. Scale bars: x: 200 ms, y: 50 μV for STA (black), 100 μV for RTA (pink). g, N wave firing and well specificity in four example CA1/CA3 principal units. Top: unit STAs and RTAs, following the plotting conventions in f. DG LFP was used in each example. Bottom: well firing rasters correspondent with each unit. Grey line: time of well entry (t = 0). SWR periods plotted as pink zones. h, CA1 and CA3 unit STAs. Color indicates voltage. For each unit, LFP (1-4 Hz) from DG, CA3, or CA2 (in decreasing order of preference) was used. Unit STAs were grouped by polarity at the time of spiking (t = 0) and sorted by the time of the local extremum (peak for positive; trough for negative) nearest the time of spiking. Units with positive voltage peaks at the time of spiking were classified as N wave-coupled. i, Well specificity distributions for CA1 and CA3 principal unit populations classified by STA. For both CA1 and CA3 populations, units with positive STAs (N wave-coupled) showed higher well specificity than units with negative STAs (mean ± s.e.m.; CA1 pos.: 0.85 ± 0.03; CA1 neg.: 0.65 ± 0.04, CA1 pos. vs. CA1 neg., p < 10-5, rank-sum; CA3 pos.: 0.77 ± 0.04; CA3 neg.: 0.53 ± 0.04, CA3 pos. vs. CA3 neg., p < 0.001, rank-sum).
Mentions: We were struck by the fact that the firing pattern of N units was not only unorthodox (Fig. 1) but also had unambiguous behavioral (Fig. 2) and representational (Fig. 3) correlates. We hypothesized that this distinctive firing was the result of an unidentified input pattern in the hippocampus. To evaluate this possibility, we calculated CA2 site (N and P) unit spike-triggered averages (STAs) of hippocampal local field potential (LFP)18, analyzing locomotor and immobility periods separately (Fig. 4a).

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