Targeted Activation of Hippocampal Place Cells Drives Memory-Guided Spatial Behavior

Robinson, Nick T. M.; Descamps, Lucie A.L.; Russell, Lloyd E.; Buchholz, Moritz O.; Bicknell, Brendan A.; Antonov, Georgy K.; Lau, Joanna; Nutbrown, Rebecca; Schmidt-Hieber, Christoph; Häusser, Michael

doi:10.1016/j.cell.2020.09.061

Cited by 200 publications

(115 citation statements)

References 107 publications

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“…From these data, a researcher could search for activity patterns that may be indicative of memory encoding and retrieval processes. Key findings from this approach have identified hippocampal spiking patterns that correlate with spatiotemporal aspects of experience ( Buzsáki and Moser, 2013 ; Buzsáki and Tingley, 2018 ; O'Keefe and Dostrovsky, 1971 ; Pastalkova et al, 2008 ), reactivate during memory retrieval ( Foster, 2017 ; Joo and Frank, 2018 ; Lee and Wilson, 2002 ) and can be causally linked to behavior ( Robinson et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

“…For example, in humans, viewing specific images reactivates the firing patterns observed during initial presentation of the stimulus ( Gelbard-Sagiv et al, 2008 ). In rodents, similar neuronal populations are reactivated upon re-exposures to familiar environments ( Guzowski et al, 1999 ; Reijmers et al, 2007 ; Rubin et al, 2015 ; Shuman et al, 2020 ; Thompson and Best, 1990 ; Ziv et al, 2013 ), and activation of neuronal populations previously activated during the initial learning will induce memory retrieval ( Liu et al, 2012 ; Ramirez et al, 2013 ; Robinson et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

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The brain in motion: How ensemble fluidity drives memory-updating and flexibility

Mau

Hasselmo

Cai

2020

eLife

105

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While memories are often thought of as flashbacks to a previous experience, they do not simply conserve veridical representations of the past but must continually integrate new information to ensure survival in dynamic environments. Therefore, ‘drift’ in neural firing patterns, typically construed as disruptive ‘instability’ or an undesirable consequence of noise, may actually be useful for updating memories. In our view, continual modifications in memory representations reconcile classical theories of stable memory traces with neural drift. Here we review how memory representations are updated through dynamic recruitment of neuronal ensembles on the basis of excitability and functional connectivity at the time of learning. Overall, we emphasize the importance of considering memories not as static entities, but instead as flexible network states that reactivate and evolve across time and experience.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The brain in motion: How ensemble fluidity drives memory-updating and flexibility

Mau

Hasselmo

Cai

2020

eLife

105

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“…Second, pushing excitation wavelengths further into the near-infrared wavelength is now possible with three-photon microscopy (Ouzounov et al, 2017), with entire new opportunities for non-invasive hippocampus imaging through the neocortex (Ouzounov et al, 2017;Weisenburger et al, 2019). Finally, the combination of multi-photon imaging with optogenetic manipulation of specific neuronal ensembles, as recently demonstrated in the CA1 region (Robinson et al, 2020), will open new avenues for all-optical interrogation of hippocampal neuronal ensemble dynamics.…”

Section: Discussionmentioning

confidence: 99%

In vivocalcium imaging of CA3 pyramidal neuron populations in adult mouse hippocampus

Schoenfeld¹,

Carta²,

Rupprecht³

et al. 2021

Preprint

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Neuronal population activity in the hippocampal CA3 subfield is implicated in cognitive brain functions such as memory processing and spatial navigation. However, because of its deep location in the brain, the CA3 area has been difficult to target with modern calcium imaging approaches. Here, we achieved chronic two-photon calcium imaging of CA3 pyramidal neurons with the red fluorescent calcium indicator R-CaMP1.07 in anesthetized and awake mice. We characterize CA3 neuronal activity at both the single-cell and population level and assess its stability across multiple imaging days. During both anesthesia and wakefulness, nearly all CA3 pyramidal neurons displayed calcium transients. Most of the calcium transients were consistent with a high incidence of bursts of action potentials, based on calibration measurements using simultaneous juxtacellular recordings and calcium imaging. In awake mice, we found state-dependent differences with striking large and prolonged calcium transients during locomotion. We estimate that trains of >30 action potentials over 3 s underlie these salient events. Their abundance in particular subsets of neurons was relatively stable across days. At the population level, we found that coactivity within the CA3 network was above chance level and that co-active neuron pairs maintained their correlated activity over days. Our results corroborate the notion of state-dependent spatiotemporal activity patterns in the recurrent network of CA3 and demonstrate that at least some features of population activity, namely coactivity of cell pairs and likelihood to engage in prolonged high activity, are maintained over days.

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“…Such evidence suggests that a change in the framework from a single cell to population analysis is mandatory to study the retinal circuits’ algorithms. Neuronal ensembles defined as groups of neurons with a coordinated activity that represent percepts, movements, or cognitive states (Carrillo-Reid and Yuste, 2020b) have recently proved useful to demonstrate the causal relationship between population activity and learned behaviors (Carrillo-Reid et al, 2019;Carrillo-Reid and Yuste, 2020a;Robinson et al, 2020), indicating that the ensemble framework could benefit the study of retinal neuronal microcircuits.…”

Section: Discussionmentioning

confidence: 99%

Parallel processing of natural images by overlapping retinal neuronal ensembles

Pérez-Ortega¹,

Araya²,

Ibaceta³

et al. 2021

Preprint

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Even though the retinal microcircuit organization has been described in detail at the single-cell level, little is known about how groups of retinal cells' coordinated activity encode and process parallel information representing the spatial and temporal structure of changing environmental conditions. To describe the population dynamics of retinal neuronal ensembles, we used microelectrode array recordings that describe hundreds of retinal ganglion cells' simultaneous activity in response to a short movie captured in the natural environment where our subject develops their visual behaviors. The vectorization of population activity allowed the identification of retinal neuronal ensembles that synchronize to specific segments of natural stimuli. These synchronous retinal neuronal ensembles were reliably activated by the same stimuli at different trials, indicating a robust population response of retinal microcircuits. The generation of asynchronous events required integrating a physiologically meaningful time window larger than 80 ms, demonstrating that retinal neuronal ensembles' time integration filters non-structured visual information. Interestingly, individual neurons could be part of several ensembles indicating that parallel circuits could encode environmental conditions changes. We conclude that parallel neuronal ensembles could represent the functional unit of retinal computations and propose that the further study of retinal neuronal ensembles could reveal emergent properties of retinal circuits that individual cells' activity cannot explain.

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Targeted Activation of Hippocampal Place Cells Drives Memory-Guided Spatial Behavior

Cited by 200 publications

References 107 publications

The brain in motion: How ensemble fluidity drives memory-updating and flexibility

The brain in motion: How ensemble fluidity drives memory-updating and flexibility

In vivocalcium imaging of CA3 pyramidal neuron populations in adult mouse hippocampus

Parallel processing of natural images by overlapping retinal neuronal ensembles

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