Reactivation predicts the consolidation of unbiased long-term cognitive maps

Grosmark, Andres; Sparks, Fraser T.; Davis, Matt J.; Losonczy, Attila

doi:10.1038/s41593-021-00920-7

Cited by 71 publications

(68 citation statements)

References 71 publications

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“…Representative waveforms and the power spectrograms of detected SWRs are shown in Figure 3A. In agreement with previous electrophysiological and optical recordings 3,11,12,22 , we clearly observed that a large number of CA1 pyramidal cells were sharply activated during the SWRs detected in the channels within FOVs (Figure 3B and C). A significant fraction of synchronous calcium events (SCEs) cooccurred with SWRs (51% SWRs to SCEs, and 35% SCEs to SWRs, Figure 3D), and SCEs were associated with a robust increase in ripple band envelope power (Figure 3E).…”

Section: In Vivo Multimodal Recordings From Hippocampal Area Ca1 With E-cannulasupporting

confidence: 90%

“…Recent studies have successfully combined local field potential recordings from the hippocampus from one hemisphere with simultaneous two-photon calcium imaging from the other hemisphere 11,12 . They reported that the SCEs in the hippocampus co-occurred with the SWR events detected in the contralateral hippocampus.…”

Section: Discussionmentioning

confidence: 99%

“…In this work, we applied the E-Cannula to obtain a dynamic map of SWRs in the CA1 region of the mouse hippocampus through simultaneous two-photon calcium imaging and direct recordings of SWR generation and propagation across the same population of cells. To date, in vivo studies into SWR-associated hippocampal neuronal dynamics have almost exclusively utilized electrophysiological recordings with single-or multiple-shank penetrating probes, with only a few instances of two-photon calcium imaging with simultaneous contralateral local field potential recordings 11,12 . Therefore, correlated spatial and temporal characteristics of SWR-related neural dynamics remain largely unknown.…”

Section: Introductionmentioning

confidence: 99%

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E-Cannula reveals anatomical diversity in sharp-wave ripples as a driver for the recruitment of distinct hippocampal assemblies

Liu

Terada

Kim

et al. 2021

Preprint

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The hippocampus plays a critical role in spatial navigation and episodic memory. However, research on in vivo hippocampal activity dynamics has mostly relied on single modalities such as electrical recordings or optical imaging, with respectively limited spatial and temporal resolution. This technical difficulty greatly impedes multi-level investigations into network state-related changes in cellular activity. To overcome these limitations, we developed the E-Cannula integrating fully transparent graphene microelectrodes with imaging-cannula. The E-Cannula enables the simultaneous electrical recording and two-photon calcium imaging from the exact same population of neurons across an anatomically extended region of the mouse hippocampal CA1 stably across several days. These large-scale simultaneous optical and electrical recordings showed that local hippocampal sharp wave ripples (SWRs) are associated with synchronous calcium events involving large neural populations in CA1. We show that SWRs exhibit spatiotemporal wave patterns along multiple axes in 2D space with different spatial extents (local or global) and temporal propagation modes (stationary or travelling). Notably, distinct SWR wave patterns were associated with, and decoded from, the selective recruitment of orthogonal CA1 cell assemblies. These results suggest that the diversity in the anatomical progression of SWRs may serve as a mechanism for the selective activation of the unique hippocampal cell assemblies extensively implicated in the encoding of distinct memories. Through these results we demonstrate the utility of the E-Cannula as a versatile neurotechnology with the potential for future integration with other optical components such as green lenses, fibers or prisms enabling the multi-modal investigation of cross-time scale population-level neural dynamics across brain regions.

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Section: In Vivo Multimodal Recordings From Hippocampal Area Ca1 With E-cannulasupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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E-Cannula reveals anatomical diversity in sharp-wave ripples as a driver for the recruitment of distinct hippocampal assemblies

Liu

Terada

Kim

et al. 2021

Preprint

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“…To calculate a measure for spatial information content for granule cells in Figure 1G , we adapted a traditional method of spatial information assessment ( Danielson et al, 2016 ; Grosmark et al, 2021 ; Skaggs et al, 1993 ) to Ca 2+ imaging data. For each cell, we used the firing rate-by-position vector and shuffled null distribution computed above and calculated the spatial information content ( Grosmark et al, 2021 ; Skaggs et al, 1993 ) as follows:

Where λ is the overall mean event rate, λ i is the mean event rate of each cell in the i th bin, p i is the probability of that mouse being in the i th bin that is occupancy in the i th bin/ 15mins.…”

Section: Discussionmentioning

confidence: 99%

Parallel processing of sensory cue and spatial information in the dentate gyrus

et al. 2022

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During exploration, animals form an internal map of an environment by combining information about landmarks and the animal's movement, a process that depends on the hippocampus. The dentate gyrus (DG) is the first stage of the hippocampal circuit where self-motion (''where'') and sensory cue information (''what'') are integrated, but it remains unknown how DG neurons encode this information during cognitive map formation. Using two-photon calcium imaging in mice running on a treadmill along with online cue manipulation, we identify robust sensory cue responses in DG granule cells. Cue cell responses are stable, stimulus-specific, and accompanied by inhibition of nearby neurons. This demonstrates the existence of ''cue cells'' in addition to better characterized ''place cells'' in the DG. We hypothesize that the DG supports parallel channels of spatial and non-spatial information that contribute distinctly to downstream computations and affect roles of the DG in spatial navigation and episodic memory.

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“…The majority of CA1 neurons change their spatial representation over time 8,27 , suggesting that a transformation of dynamic-to-stable neuronal responses might occur during this passage of spatial information to the mPFC network. Alternatively, a subset of CA1 place cells with temporally consistent place field locations 28 , or spatially tuned neurons in other neocortical areas such as somatosensory 29 or orbitofrontal cortex 30 might support stable spatial tuning in mPFC circuits. The cellular and network processes which might underlie the transmission of spatial information remain, however, to be investigated.…”

Section: Discussionmentioning

confidence: 99%

A persistent prefrontal reference frame across time and task rules

Muysers

Chen

Sauer

et al. 2022

Preprint

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Behavior can be remarkably consistent, even over extended time periods, yet whether this is reflected in stable or ‘drifting’ neuronal responses to task features remains controversial. We find a persistently active ensemble of neurons in the medial prefrontal cortex (mPFC) of mice that reliably maintains trajectory-specific tuning over several weeks of performance in an olfaction-guided spatial memory task. The spatial map is stabilized during learning, upon which repeatedly active neurons show little representational drift and maintain their spatial tuning across long pauses in task exposure and across repeated changes in cue-target location pairings. These data thus suggest a ‘core ensemble’ of prefrontal neurons forming a reference frame of task-relevant space for the performance of consistent behavior over extended periods of time.

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Reactivation predicts the consolidation of unbiased long-term cognitive maps

Cited by 71 publications

References 71 publications

E-Cannula reveals anatomical diversity in sharp-wave ripples as a driver for the recruitment of distinct hippocampal assemblies

E-Cannula reveals anatomical diversity in sharp-wave ripples as a driver for the recruitment of distinct hippocampal assemblies

Parallel processing of sensory cue and spatial information in the dentate gyrus

A persistent prefrontal reference frame across time and task rules

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