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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.

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Observation of firing during immobilitya, Non-SWR immobility firing in three example principal units recorded in CA1, CA2, and CA3. Each firing raster is shown as vertical lines overlaid on a plot of the subject's head speed (grey trace). Top traces: wide-band LFP (0.5-400 Hz, scale bar: 800 μV) and ripple-band LFP (150-250 Hz, scale bar: 100 μV) traces from a simultaneous recording in CA1, to show hippocampal network state. SWR periods are plotted as pink zones. Note that substantial firing occurs in the absence of (i) locomotion, (ii) detectable SWRs, and (iii) detectable theta (regular ∼8 Hz rhythm visible in the LFP during moving periods). b, Proportions of time spent in different period types over all task recording epochs (n = 222 task recording epochs, 8 subjects) in the data set. During the performance of the task, a substantial proportion of time was spent at low speeds and immobility, moreover when SWRs were not detected. Transitional low speed periods were times when the subject's speed was <4 cm/s and within 2 s (earlier or later) of periods of movement >4 cm/s, while immobility periods were times when the speed was <4 cm/s but separated more than 2 s (earlier or later) from periods of movement >4 cm/s. Note that SWR periods comprised only a minority of time spent at low speeds, consistent with past observations17,71,72.
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Figure 2: Observation of firing during immobilitya, Non-SWR immobility firing in three example principal units recorded in CA1, CA2, and CA3. Each firing raster is shown as vertical lines overlaid on a plot of the subject's head speed (grey trace). Top traces: wide-band LFP (0.5-400 Hz, scale bar: 800 μV) and ripple-band LFP (150-250 Hz, scale bar: 100 μV) traces from a simultaneous recording in CA1, to show hippocampal network state. SWR periods are plotted as pink zones. Note that substantial firing occurs in the absence of (i) locomotion, (ii) detectable SWRs, and (iii) detectable theta (regular ∼8 Hz rhythm visible in the LFP during moving periods). b, Proportions of time spent in different period types over all task recording epochs (n = 222 task recording epochs, 8 subjects) in the data set. During the performance of the task, a substantial proportion of time was spent at low speeds and immobility, moreover when SWRs were not detected. Transitional low speed periods were times when the subject's speed was <4 cm/s and within 2 s (earlier or later) of periods of movement >4 cm/s, while immobility periods were times when the speed was <4 cm/s but separated more than 2 s (earlier or later) from periods of movement >4 cm/s. Note that SWR periods comprised only a minority of time spent at low speeds, consistent with past observations17,71,72.

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
Observation of firing during immobilitya, Non-SWR immobility firing in three example principal units recorded in CA1, CA2, and CA3. Each firing raster is shown as vertical lines overlaid on a plot of the subject's head speed (grey trace). Top traces: wide-band LFP (0.5-400 Hz, scale bar: 800 μV) and ripple-band LFP (150-250 Hz, scale bar: 100 μV) traces from a simultaneous recording in CA1, to show hippocampal network state. SWR periods are plotted as pink zones. Note that substantial firing occurs in the absence of (i) locomotion, (ii) detectable SWRs, and (iii) detectable theta (regular ∼8 Hz rhythm visible in the LFP during moving periods). b, Proportions of time spent in different period types over all task recording epochs (n = 222 task recording epochs, 8 subjects) in the data set. During the performance of the task, a substantial proportion of time was spent at low speeds and immobility, moreover when SWRs were not detected. Transitional low speed periods were times when the subject's speed was <4 cm/s and within 2 s (earlier or later) of periods of movement >4 cm/s, while immobility periods were times when the speed was <4 cm/s but separated more than 2 s (earlier or later) from periods of movement >4 cm/s. Note that SWR periods comprised only a minority of time spent at low speeds, consistent with past observations17,71,72.
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Related In: Results  -  Collection

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Figure 2: Observation of firing during immobilitya, Non-SWR immobility firing in three example principal units recorded in CA1, CA2, and CA3. Each firing raster is shown as vertical lines overlaid on a plot of the subject's head speed (grey trace). Top traces: wide-band LFP (0.5-400 Hz, scale bar: 800 μV) and ripple-band LFP (150-250 Hz, scale bar: 100 μV) traces from a simultaneous recording in CA1, to show hippocampal network state. SWR periods are plotted as pink zones. Note that substantial firing occurs in the absence of (i) locomotion, (ii) detectable SWRs, and (iii) detectable theta (regular ∼8 Hz rhythm visible in the LFP during moving periods). b, Proportions of time spent in different period types over all task recording epochs (n = 222 task recording epochs, 8 subjects) in the data set. During the performance of the task, a substantial proportion of time was spent at low speeds and immobility, moreover when SWRs were not detected. Transitional low speed periods were times when the subject's speed was <4 cm/s and within 2 s (earlier or later) of periods of movement >4 cm/s, while immobility periods were times when the speed was <4 cm/s but separated more than 2 s (earlier or later) from periods of movement >4 cm/s. Note that SWR periods comprised only a minority of time spent at low speeds, consistent with past observations17,71,72.
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.


Related in: MedlinePlus