Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments

Cohen, Jack B.; Bolstad, Mark; Lee, Albert K.

doi:10.7554/elife.23040

Cited by 123 publications

(194 citation statements)

References 100 publications

(195 reference statements)

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“…The long-term stabilization of the place code for a given environment would then depend on plasticity, which could involve regenerative dendritic spikes or plateau potentials—large calcium-mediated complex spike events [13 •• ,63,71 • ]. This idea is consistent with newer research indicating that plateau potentials are not necessary for the formation of fields but contribute to their long-term stabilization [72 • ]. Variability in place cell stability seen, for example, in superficial versus deep layers could then arise from differences in single-cell biophysics that render the conditions for a plateau potential induction more or less favorable.…”

Section: Introductionsupporting

confidence: 57%

Heterogeneity in hippocampal place coding

Mallory

Giocomo

2018

Current Opinion in Neurobiology

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The discovery of place cells provided fundamental insight into the neural basis by which the hippocampus encodes spatial memories and supports navigation and prompted the development of computational models to explain the emergence of their spatial selectively. Many such works posit that input from entorhinal grid cells is critical to the formation of place fields, a prediction that has received mixed experimental support. Potentially reconciling seemingly conflicting findings is recent work indicating that subpopulations of pyramidal neurons are functionally distinct and may be driven to varying degrees by different inputs. Additionally, new studies have demonstrated that hippocampal principal neurons encode a myriad of features extending beyond current position. Here, we highlight recent evidence for how extensive heterogeneity in connectivity and genetic expression could interact with membrane biophysics to enable place cells to encode a diverse range of stimuli. These recent findings highlight the need for more computational models that integrate these heterogeneous features of hippocampal principal neurons.

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Section: Introductionsupporting

confidence: 57%

Heterogeneity in hippocampal place coding

Mallory

Giocomo

2018

Current Opinion in Neurobiology

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“…Our findings are consistent with a model in which a new environment is associated with decreased network inhibition which then gradually recovers over the course of learning to stabilize the network, possibly via synaptic plasticity (Cohen et al, 2017;Wilson and McNaughton, 1993). We tie inhibitory suppression to learning in two ways.…”

Section: Discussionsupporting

confidence: 89%

Structured Inhibitory Activity Dynamics During Learning

Arriaga¹,

Han²

2019

Preprint

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Hippocampal network activity is tightly regulated by local inhibitory interneurons. Suppression of inhibition has been proposed to accelerate learning by enhancing network activity and plasticity; however, the activity dynamics of hippocampal interneurons during learning remain poorly understood. Furthermore, it is unknown if individual interneurons are stochastically suppressed across different learning episodes, mirroring the random remapping of place cells, or if instead they exhibit consistent patterns of activity suppression. These critical properties define how inhibition shapes and controls learning at a network level. To uncover the functional circuit dynamics of inhibition during novelty-induced learning, we recorded calcium activity from hippocampal CA1 interneurons using two-photon imaging as mice learned a virtual reality (VR) goal-directed spatial navigation task in new visual contexts. Here we focused on dendritetargeting somatostatin-expressing interneurons (SOM-ints), which powerfully control burst firing and synaptic plasticity in excitatory neurons. We found robust activity suppression in SOM-ints upon exposure to novel virtual environments; activity then recovered over repeated exposures to the novel environment as the animal learned goal locations. At a population level, we found a continuum of activity suppression, from interneurons strongly suppressed to moderately activated during learning. Surprisingly, each interneuron exhibited a stable level of activity modulation: when animals were switched into a second novel environment, the magnitude of activity suppression was strongly correlated across remapping sessions. This work reveals dynamic inhibition suppression triggered by novel environments and the gradual return of inhibition with learning. Furthermore, unlike the stochastic remapping of place cells, inhibitory networks display a stable activity structure across learning episodes. This functional inhibitory circuit architecture suggests that individual interneurons play specialized and stereotyped roles during learning, perhaps by differentially regulating pyramidal subnetworks specialized for plasticity and stability.

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“…Our observation are consistent with these predictions, and part of the delay period that we observed in some place fields could be due to the time required for long term potentiation to fully take effect (Hardie and Spruston, 2009; Murakoshi et al, 2011; Tigaret et al, 2016). This idea is partly supported by a recent somatic intracellular place cell recording study that found increasing sub threshold responses in novel virtual environments before somatic place field firing began (Cohen et al, 2017). …”

Section: Discussionmentioning

confidence: 85%

Increased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation

Sheffield

Adoff

Dombeck

2017

Neuron

177

210

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Summary Hippocampal place cell ensembles form a cognitive map of space during exposure to novel environments. However, surprisingly little evidence exists to support the idea that synaptic plasticity in place cells is involved in forming new place fields. Here we used high-resolution functional imaging to determine the signaling patterns in CA1 soma, dendrites and axons associated with place field formation when mice are exposed to novel virtual environments. We found that putative local dendritic spikes often occur prior to somatic place field firing. Subsequently, the first occurrence of somatic place field firing was associated with widespread regenerative dendritic events, which decreased in prevalence with increased novel environment experience. This transient increase in regenerative events was likely facilitated by a reduction in dendritic inhibition. Since regenerative dendritic events can provide the depolarization necessary for Hebbian potentiation, these results suggest that activity dependent synaptic plasticity underlies the formation of many CA1 place fields.

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Experience-dependent shaping of hippocampal CA1 intracellular activity in novel and familiar environments

Cited by 123 publications

References 100 publications

Heterogeneity in hippocampal place coding

Heterogeneity in hippocampal place coding

Structured Inhibitory Activity Dynamics During Learning

Increased Prevalence of Calcium Transients across the Dendritic Arbor during Place Field Formation

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