Prefrontal–hippocampal pathways underlying inhibitory control over memory

Anderson, Michael C.; Bunce, Jamie G.; Barbas, Helen

doi:10.1016/j.nlm.2015.11.008

Cited by 190 publications

(194 citation statements)

References 173 publications

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“…Cognitive alterations resulting from experimental manipulations of RE (i.e., lesions, reversible inactivation, optogenetic stimulation) support the idea that, instead of specifically affecting the functioning of either the mPFC or hippocampus, RE is mainly involved in orchestrating the flow of hippocampal-mPFC information, likely by modulating the coupling between both structures (Viana di Prisco and Vertes 2006;Saalmann 2014;Cassel and 4 Pereira Ito et al 2015;Pereira de Vasconcelos and Cassel 2015). The EC has also been shown to play a role in various cognitive tasks (e.g., Skelton and McNamara 1992;Sybirska et al 2000;Remondes and Schumann 2004;Brun et al 2008;Deshmuk and Knierum 2011;Suh et al 2011;Wilson et al 2013;Chao et al 2015;Anderson et al 2015), and both RE and EC appear to be involved in the consolidation of hippocampal-dependent memories (Remondes and Schumann 2004;Loureiro et al 2012). Moreover, Xu and Sűdhof (2013) have proposed that the cooperativity between RE-CA1 and EC-CA1 input may reduce the threshold for synaptic plasticity, and thus for the incorporation of entorhinal-transmitted neocortical information in hippocampal memory representation and subsequent long-term storage.…”

Section: Introductionmentioning

confidence: 84%

“…Recent studies have indicated the importance of RE for cognitive processes, such as behavioural flexibility, strategy shifting, inhibitory response control, associative learning, memory consolidation, working memory, fear memory, memory generalization, goal-directed navigation, and executive behaviours (Dollemanvan der Weel et al 2009;Davoodi et al 2011;Eleore et al 2011;Hembrook et al 2011;Kincheski et al 2012;Loureiro et al 2012;Cholvin et al 2013;Hallock et al 2013;Prasad et al 2013;Varela et al 2013;Wheeler et al 2013;Xu and Sűdhof 2013;Duan et al 2015;Griffin 2015;Ito et al 2015;Layfield et al 2015;Anderson et al 2015;Prasad et al 2016). This variety of memory-related behaviours has also been associated with the interplay between the medial prefrontal cortex (mPFC) and the hippocampus (Jin and Maren 2015).…”

Section: Introductionmentioning

confidence: 99%

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Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Weel

Silva

2016

Brain Struct Funct

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The nucleus reuniens (RE) and entorhinal cortex (EC) provide monosynaptic excitatory inputs to the apical dendrites of pyramidal cells and to interneurons with dendrites in stratum lacunosum-moleculare (LM) of hippocampal field CA1. However, whether the RE and EC inputs interact at the cellular level is unknown. In this electrophysiological in vivo study, low frequency stimulation was used to selectively activate each projection at its origin; field excitatory postsynaptic potentials (fEPSPs) were recorded in CA1. We applied 1) paired pulses to RE or EC, 2) combined paired pulses to RE and EC, and 3) simultaneously paired pulses to RE/EC. The main findings are that: i) stimulation of either RE or EC evoked subthreshold fEPSPs, displaying paired pulse facilitation (PPF), ii) subthreshold fEPSPs evoked by combined stimulation did not display heterosynaptic PPF, and iii) simultaneous stimulation of RE/EC resulted in enhanced subthreshold fEPSPs in proximal LM displaying a nonlinear interaction.CSD analyses of RE/EC-evoked depth profiles revealed a nonlinear enlargement of the 'LM sink-radiatum source' configuration and the appearance of an additional small sink-source pair close to stratum pyramidale, likely reflecting (peri)somatic inhibition. The nonlinear interaction between both inputs indicates that RE and EC axons form synapses, at least partly, onto the same dendritic compartments of CA1 pyramidal cells. We propose that low frequency activation of the RE-CA1 input facilitates the entorhinal-hippocampal dialogue, and may synchronize the neocortical-hippocampal slow oscillation which is relevant for hippocampal-dependent memory consolidation.

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Section: Introductionmentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Weel

Silva

2016

Brain Struct Funct

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“…Given these observations, we suggest that the hippocampus contributes to selective inhibition of neocortical inhibitory engrams, providing a means to reactivate otherwise silent memories by selectively modulating EI balance in favor of excitation. On the other hand, the PFC is thought to be critical for directed forgetting (55) and may exert further top-down control over the hippocampus to prevent involuntary memory recall (53,56). Selective disinhibition, via the hippocampus or PFC, may be particularly critical when so-called "inhibitory control" is necessary to prevent recall following exposure to a cue that has the potential to trigger an unwanted memory (55).…”

Section: Inhibitory Engrams In Associative Memory Storage and Recallmentioning

confidence: 99%

“…On the other hand, the PFC is thought to be critical for directed forgetting (55) and may exert further top-down control over the hippocampus to prevent involuntary memory recall (53,56). Selective disinhibition, via the hippocampus or PFC, may be particularly critical when so-called "inhibitory control" is necessary to prevent recall following exposure to a cue that has the potential to trigger an unwanted memory (55). We further speculate that the precise contribution made by these two brain regions may depend on the age of a memory, with disinhibition for recent and remote memories showing greater dependence upon the hippocampus and PFC, respectively (57)(58)(59).…”

Section: Inhibitory Engrams In Associative Memory Storage and Recallmentioning

confidence: 99%

Inhibitory engrams in perception and memory

Barron

Vogels

Behrens

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

135

126

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Nervous systems use excitatory cell assemblies to encode and represent sensory percepts. Similarly, synaptically connected cell assemblies or "engrams" are thought to represent memories of past experience. Multiple lines of recent evidence indicate that brain systems create and use inhibitory replicas of excitatory representations for important cognitive functions. Such matched "inhibitory engrams" can form through homeostatic potentiation of inhibition onto postsynaptic cells that show increased levels of excitation. Inhibitory engrams can reduce behavioral responses to familiar stimuli, thereby resulting in behavioral habituation. In addition, by preventing inappropriate activation of excitatory memory engrams, inhibitory engrams can make memories quiescent, stored in a latent form that is available for contextrelevant activation. In neural networks with balanced excitatory and inhibitory engrams, the release of innate responses and recall of associative memories can occur through focused disinhibition. Understanding mechanisms that regulate the formation and expression of inhibitory engrams in vivo may help not only to explain key features of cognition but also to provide insight into transdiagnostic traits associated with psychiatric conditions such as autism, schizophrenia, and posttraumatic stress disorder.Percepts are thought to be represented in the brain by excitatory activity in groups of neurons, described as cell assemblies (1). Memories may similarly be represented by excitatory connections across different cell assemblies, which form when experiences trigger coordinated activity. Several recent studies indicate that the storage and reactivation of these excitatory "engrams" (2), respectively, may be accompanied by creation and modulation of matched inhibitory engrams. Here, we propose that inhibitory engrams, also termed "negative images" or "inhibitory representations," explain two fundamental features of animal and human psychology: first, behavioral habituation, which allows organisms to ignore familiar, frequently encountered percepts or stimuli, and, second, latent memory, wherein the brain stores tens of thousands of memories in a silent or latent state until recall is required. Such inhibitory engrams can be constructed in neural networks through simple, evolutionarily primitive, synaptic and cellular mechanisms, which are recognized to be involved in the phenomenon of excitatory-inhibitory (EI) balance observed across the brain.Neurons and neural circuits normally operate within a preset range of activity. Outside this range, altered levels of neuronal spiking trigger a variety of homeostatic mechanisms ranging from compensatory ion channel expression to local synaptic scaling (3, 4). These homeostatic mechanisms ensure that the activity parameters of a neuron operate around a set point such that the spiking rates remain stable and a balance of depolarizing and hyperpolarizing currents is maintained. As a consequence, excitation and inhibition are both locally and globally balanced, despite...

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“…For example, reactivation within posterior parietal cortex (PPC) reflects detailed information about retrieved content (Kuhl and Chun, 2014;Lee et al, 2016). Reactivation within medial prefrontal cortex (mPFC) is thought to be of particular importance when past experience is compared with present experience (Kroes and Fernandez, 2012;Schlichting and Preston, 2015;Demblon et al, 2016;Richter et al, 2016) and connections between mPFC and hippocampus may provide the ideal scaffolding for a prediction generation and comparison system (Preston and Eichenbaum, 2013;Rajasethupathy et al, 2015;Anderson et al, 2016). Collectively, PPC and mPFC are part of the brain's so-called default mode network (DMN) and it has been argued that the DMN plays a central role in memory-based predictions (Bar, 2007(Bar, , 2009.…”

Section: Introductionmentioning

confidence: 99%

Hippocampal Mismatch Signals Are Modulated by the Strength of Neural Predictions and Their Similarity to Outcomes

2016

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The hippocampus is thought to compare predicted events with current perceptual input, generating a mismatch signal when predictions are violated. However, most prior studies have only inferred when predictions occur without measuring them directly. Moreover, an important but unresolved question is whether hippocampal mismatch signals are modulated by the degree to which predictions differ from outcomes. Here, we conducted a human fMRI study in which subjects repeatedly studied various word-picture pairs, learning to predict particular pictures (outcomes) from the words (cues). After initial learning, a subset of cues was paired with a novel, unexpected outcome, whereas other cues continued to predict the same outcome. Critically, when outcomes changed, the new outcome was either "near" to the predicted outcome (same visual category as the predicted picture) or "far" from the predicted outcome (different visual category). Using multivoxel pattern analysis, we indexed cue-evoked reactivation (prediction) within neocortical areas and related these trial-by-trial measures of prediction strength to univariate hippocampal responses to the outcomes. We found that prediction strength positively modulated hippocampal responses to unexpected outcomes, particularly when unexpected outcomes were close, but not identical, to the prediction. Hippocampal responses to unexpected outcomes were also associated with a tradeoff in performance during a subsequent memory test: relatively faster retrieval of new (updated) associations, but relatively slower retrieval of the original (older) associations. Together, these results indicate that hippocampal mismatch signals reflect a comparison between active predictions and current outcomes and that these signals are most robust when predictions are similar, but not identical, to outcomes.

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Prefrontal–hippocampal pathways underlying inhibitory control over memory

Cited by 190 publications

References 173 publications

Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

Inhibitory engrams in perception and memory

Hippocampal Mismatch Signals Are Modulated by the Strength of Neural Predictions and Their Similarity to Outcomes

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