Signatures of rapid plasticity in hippocampal CA1 representations during novel experiences

Priestley, James B.; Bowler, John C; Rolotti, Sebi V.; Fusi, Stefano; Losonczy, Attila

doi:10.1016/j.neuron.2022.03.026

Cited by 79 publications

(117 citation statements)

References 78 publications

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“…In the past, we have observed that optogenetic inhibition of EC3 input reduces plateau potential initiation in CA1 cells 16 . There is considerable data, presented here and previously, showing that plateau potentials induce BTSP and place field formation 7,12,13,[16][17][18][19]45,46 . Finally, we now report that inhibition of EC3 input reduces place field formation and alters experience-dependent shaping of CA1 representations.…”

Section: Discussionmentioning

confidence: 56%

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Entorhinal cortex directs learning-related changes in CA1 representations

Grienberger

Magee

2022

Nature

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Learning-related changes in brain activity are thought to underlie adaptive behaviours1,2. For instance, the learning of a reward site by rodents requires the development of an over-representation of that location in the hippocampus3–6. How this learning-related change occurs remains unknown. Here we recorded hippocampal CA1 population activity as mice learned a reward location on a linear treadmill. Physiological and pharmacological evidence suggests that the adaptive over-representation required behavioural timescale synaptic plasticity (BTSP)7. BTSP is known to be driven by dendritic voltage signals that we proposed were initiated by input from entorhinal cortex layer 3 (EC3). Accordingly, the CA1 over-representation was largely removed by optogenetic inhibition of EC3 activity. Recordings from EC3 neurons revealed an activity pattern that could provide an instructive signal directing BTSP to generate the over-representation. Consistent with this function, our observations show that exposure to a second environment possessing a prominent reward-predictive cue resulted in both EC3 activity and CA1 place field density that were more elevated at the cue than at the reward. These data indicate that learning-related changes in the hippocampus are produced by synaptic plasticity directed by an instructive signal from the EC3 that seems to be specifically adapted to the behaviourally relevant features of the environment.

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Section: Discussionmentioning

confidence: 56%

“…1). These suddenly appearing place fields exhibited additional hallmark features of BTSP 12,19 . First, place fields tended to shift backwards in space compared to the activity in their induction lap (Fig.…”

mentioning

confidence: 97%

Entorhinal cortex directs learning-related changes in CA1 representations

Grienberger

Magee

2022

Nature

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“…The rapid neural response upon exposure to a novel environment, pointed by the red arrow in Fig. 3B, is a well established place cell property called one-shot plasticity [26], whose mechanism is still debatable. Scientists have been looking for plasticity principles that modify weight abruptly [27], which might be dangerous for maintaining system stability if loosely regulated.…”

Section: Resultsmentioning

confidence: 99%

Predictive Sequence Learning in the Hippocampal Formation

Chen

Zhang

Sejnowski

2022

Preprint

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The interaction between hippocampus and cortex is key to memory formation and representation learning. Based on anatomical wiring and transmission delays, we proposed a self-supervised recurrent neural network (PredRAE) with a predictive reconstruction loss to account for the cognitive functions of hippocampus. This framework extends predictive coding in the time axis and incorporates predictive features in Bayes filters for temporal prediction. In simulations, we were able to reproduce characteristic place cell features such as one-shot plasticity, localized spatial representation and replay, which marks the trace of memory formation. The simulated place cells also exhibited precise spike timing, evidenced by phase precession. Trained on MNIST sequences, PredRAE learned the underlying temporal dependencies and a spontaneous representation of digit labels and rotation dynamics in the linear transformation of its hidden unit activities. Such learning is robust against 16 different image corruptions. Inspired by the brain circuit, the simple and concise framework has great potential to approximate human performance with its capacity to robustly disentangle representations and generalize temporal dynamics.

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Section: Discussionmentioning

confidence: 99%

“…Indeed, if the increased synaptic strength onto photoconverted superficial neurons represented a pre-existing state, it is difficult to explain the significant changes we observe in the firing rates of individual superficial neurons from pre- to post-experience SWRs. Finally, considerable evidence supports a role for in vivo synaptic plasticity in the formation of place fields during active navigation and the establishment of stable spatial representation across the hippocampal network 6–9,20–22,66 , arguing that experience can induce synaptic plasticity in vivo . Thus, while we leave open the possibility that the synaptic differences we observe between photoconverted and unconverted neurons reflect pre-existing phenotypes, we interpret these findings as plasticity-induced changes driven by in vivo activity during experience.…”

Section: Discussionmentioning

confidence: 99%

Bidirectional synaptic changes in deep and superficial hippocampal neurons followingin vivoactivity

Berndt

Trusel

Roberts

et al. 2022

Preprint

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Neuronal activity during experience is thought to induce plastic changes within the hippocampal network which underlie memory formation, although the extent and details of such changes in vivo remain unclear. Here, we employed a temporally precise marker of neuronal activity, CaMPARI2, to label active CA1 hippocampal neurons in vivo, followed by immediate acute slice preparation and electrophysiological quantification of synaptic properties. Recently active neurons in the superficial sublayer of stratum pyramidale displayed larger post-synaptic responses at excitatory synapses from area CA3, with no change in pre-synaptic release probability. In contrast, in vivo activity weakened both pre- and post-synaptic excitatory weights onto pyramidal cells in the deep sublayer. In vivo activity of deep and superficial neurons within sharp-wave ripples was bidirectionally changed across experience, consistent with the observed changes in synaptic weights. These findings reveal novel, fundamental mechanisms through which the hippocampal network is modified by experience to store information.

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Signatures of rapid plasticity in hippocampal CA1 representations during novel experiences

Cited by 79 publications

References 78 publications

Entorhinal cortex directs learning-related changes in CA1 representations

Entorhinal cortex directs learning-related changes in CA1 representations

Predictive Sequence Learning in the Hippocampal Formation

Bidirectional synaptic changes in deep and superficial hippocampal neurons followingin vivoactivity

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