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.2020.12.010

Cited by 71 publications

(88 citation statements)

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“…On any given trial though, we hypothesized that the locations of new place fields might be constrained by the representation assembled over prior laps. This could arise from the recruitment of lateral inhibition at locations with existing place fields (Rolotti et al 2021, Milstein et al 2020, Robinson et al 2020), promoting competitive interactions that repel accumulating fields away from one another. The result would be that the spatial distribution of new fields on a given lap is not purely random but is also conditional on the location of recently acquired fields.…”

Section: Resultsmentioning

confidence: 99%

“…We found that place fields forming via BTSP were generally less precise than the remaining fields (Figure S8). While many neurons may first reach threshold via BTSP, it seems likely that this initial tuning is refined through secondary mechanisms, such as conventional Hebbian rules and local competitive interactions with other pyramidal neurons mediated through lateral inhibition (Mehta et al 2000, Cohen et al 2017, McKenzie et al 2021, Robinson et al 2020). Considering that many of the non-BTSP fields are pre-existing place fields learned during previous experience, this could explain why BTSP fields were consistently wider, having not yet undergone further refinement.…”

Section: Discussionmentioning

confidence: 99%

“…While here we focused on overall environmental novelty, the hippocampal place code is also heavily influenced by the density and salience of environmental cues (Manns & Eichenbaum 2009,Bourboulou et al 2019) and the presence of reinforcement (Hollup et al 2001, Zaremba et al 2017, Dupret et al 2010), representations of which may actively shape behavior (Robinson et al 2020). We searched for evidence of differential concentration of BTSP-like field formation along the virtual track, but found that the distribution was mainly uniform over space after regressing out the component correlated with velocity (Figure 6).…”

Section: Discussionmentioning

confidence: 99%

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Signatures of rapid synaptic learning in the hippocampus during novel experiences

Priestley

Bowler

Rolotti

et al. 2021

Preprint

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Neurons in the hippocampus exhibit striking selectivity for specific combinations of sensory features, forming representations which are thought to subserve episodic memory. Even during a completely novel experience, ensembles of hippocampal ``place cells'' are rapidly configured such that the population sparsely encodes visited locations, stabilizing within minutes of the first exposure to a new environment. What cellular mechanisms enable this fast encoding of experience? Here we leverage virtual reality and large scale neural recordings to dissect the effects of novelty and experience on the dynamics of place field formation. We show that the place fields of many CA1 neurons transiently shift locations and modulate the amplitude of their activity immediately after place field formation, consistent with rapid plasticity mechanisms driven by plateau potentials and somatic burst spiking. These motifs were particularly enriched during initial exploration of a novel context and decayed with experience. Our data suggest that novelty modulates the effective learning rate in CA1, favoring burst-driven field formation to support fast synaptic updating during new experience.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Signatures of rapid synaptic learning in the hippocampus during novel experiences

Priestley

Bowler

Rolotti

et al. 2021

Preprint

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“…Efficient expression of all-optical constructs should result in hundreds of neurons in a single field-of-view (i.e. 500 µm x 500 µm) which are coexpressing enough opsin and indicator for photostimulation and readout (see -Reid et al, 2016-Reid et al, , 2019Chettih and Harvey, 2019;Jennings et al, 2019;Marshel et al, 2019;Russell et al, 2019;Dalgleish et al, 2020;Robinson et al, 2020;Daie et al, 2021).…”

Section: Anticipated Resultsmentioning

confidence: 99%

All-optical interrogation of neural circuits in behaving mice

Russell

Dalgleish

Nutbrown

et al. 2021

Preprint

Self Cite

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Recent advances combining two-photon calcium imaging and two-photon optogenetics with digital holography now allow us to read and write neural activity in vivo at cellular resolution with millisecond temporal precision. Such 'all-optical' techniques enable experimenters to probe the impact of functionally defined neurons on neural circuit function and behavioural output with new levels of precision. This protocol describes the experimental strategy and workflow for successful completion of typical all-optical interrogation experiments in awake, behaving head-fixed mice. We describe modular procedures for the setup and calibration of an all-optical system, the preparation of an indicator and opsin-expressing and task-performing animal, the characterization of functional and photostimulation responses and the design and implementation of an all-optical experiment. We discuss optimizations for efficiently selecting and targeting neuronal ensembles for photostimulation sequences, as well as generating photostimulation response maps from the imaging data that can be used to examine the impact of photostimulation on the local circuit. We demonstrate the utility of this strategy using all-optical experiments in three different brain areas - barrel cortex, visual cortex and hippocampus - using different experimental setups. This approach can in principle be adapted to any brain area for all-optical interrogation experiments to probe functional connectivity in neural circuits and for investigating the relationship between neural circuit activity and behaviour.

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“…These maps are implemented by the inputs of different senses, both visual and non-visual, such as the magnetic or the olfactory ones. The neural basis of the cognitive map is represented by the activity of hippocampal place cells that support spatial navigation and memory (Robinson et al 2020). Other brain areas involved in orientation are the postero-dorso-lateral neostriatum, the pyriform cortex and the so-called "Cluster N" of the anterior forebrain Wulst.…”

Section: Natale Emilio Baldaccinimentioning

confidence: 99%

Moving towards a far-away goal: a foreword

Baldaccini

2021

Ethology Ecology & Evolution

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

Cited by 71 publications

References 0 publications

Signatures of rapid synaptic learning in the hippocampus during novel experiences

Signatures of rapid synaptic learning in the hippocampus during novel experiences

All-optical interrogation of neural circuits in behaving mice

Moving towards a far-away goal: a foreword

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