Hippocampal remapping as hidden state inference

Sanders, Honi; Wilson, Matthew A.; Gershman, Samuel J.

doi:10.7554/elife.51140

Cited by 121 publications

(89 citation statements)

References 113 publications

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“…One could imagine that learning would be more likely to generalise if different neurons were activated on each training day (as in our experiments), or even each trial, than if just one pattern was trained for the same duration. Such volatility in the learning environment is indeed thought to change learning dynamics ( Behrens et al, 2007 ; Massi et al, 2018 ; McGuire et al, 2014 ) and by extension may influence the level of generalisation at the neural level, as has recently been suggested for hippocampal representations ( Plitt and Giocomo, 2019 ; Sanders et al, 2020 ).…”

Section: Discussionmentioning

confidence: 86%

How many neurons are sufficient for perception of cortical activity?

Dalgleish

Russell

Packer

et al. 2020

eLife

104

123

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Many theories of brain function assume that information is encoded and behaviour is controlled through sparse, distributed patterns of activity. It is therefore crucial to place a lower bound on the amount of neural activity that can drive behaviour and to understand how neuronal networks operate within these constraints. We use an all-optical approach to test this lower limit by driving behaviour with targeted two-photon optogenetic activation of small ensembles of L2/3 pyramidal neurons in mouse barrel cortex while using two-photon calcium imaging to record the impact on the local network. By precisely titrating the number of neurons in activated ensembles we demonstrate that the lower bound for detection of cortical activity is ~14 pyramidal neurons. We show that there is a very steep sigmoidal relationship between the number of activated neurons and behavioural output, saturating at only ~37 neurons, and that this relationship can shift with learning. By simultaneously measuring activity in the local network, we show that the activation of stimulated ensembles is balanced by the suppression of neighbouring neurons. This surprising behavioural sensitivity in the face of potent network suppression supports the sparse coding hypothesis and suggests that perception of cortical activity balances a trade-off between minimizing the impact of noise while efficiently detecting relevant signals.

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Section: Discussionmentioning

confidence: 86%

How many neurons are sufficient for perception of cortical activity?

Dalgleish

Russell

Packer

et al. 2020

eLife

104

123

View full text Add to dashboard Cite

show abstract

“…This implies an important role for affective input in schema-forming and updates, for both rewarding and aversive experiences (Phelps and LeDoux, 2005 ; Tonegawa et al, 2018 ). Based on Talmi et al ( 2019 ), all naturally related and all affectively similar or similarly intense episodic memories tend to cross-promote each other by semantic (top-down) or by affective (bottom-up) stimuli, which may be objective or based on subjective inference (Sanders et al, 2020 ). The en masse activation may involve either real-time stimuli or may occur internally, by default mode processing which enables a person to time-travel through memories and their associated affects.…”

Section: Neuroscience Of Key Psychoanalytic Postulates About Object Rmentioning

confidence: 99%

“…Remapping of hippocampal engrams that encode context and content reflects subjective beliefs about the hidden states of environment (“hidden state inference”), rather than objective, observable properties of the environment (Sanders et al, 2020 ). Hidden states are inferred from observations that are based on and thus also biased by prior experience (safety, danger).…”

Section: Neuroscience Of Psychodynamic Psychotherapymentioning

confidence: 99%

“…Hidden states are inferred from observations that are based on and thus also biased by prior experience (safety, danger). The regularity of a hidden state can be learned over the course of experience, leading to increased certainty about hidden state assignments (Sanders et al, 2020 ).…”

Section: Neuroscience Of Psychodynamic Psychotherapymentioning

confidence: 99%

“…Such generalization is possible because the master schema of early object relations is not object-specific but experience-specific, as episodic memories of particular events have been forgotten. Negative experiences may be discriminated against as early as at the level of hippocampus-amygdala processing (Sun et al, 2020 ), and may lead to increased certainty of assignments about hidden state of the environment (Sanders et al, 2020 ), now expected to be positive.…”

Section: Neuroscience Of Psychodynamic Psychotherapymentioning

confidence: 99%

See 2 more Smart Citations

Neuroscience of Object Relations in Health and Disorder: A Proposal for an Integrative Model

Švrakić

Zorumski

2021

Front. Psychol.

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Recent advances in the neuroscience of episodic memory provide a framework to integrate object relations theory, a psychoanalytic model of mind development, with potential neural mechanisms. Object relations are primordial cognitive-affective units of the mind derived from survival- and safety-level experiences with caretakers during phase-sensitive periods of infancy and toddlerhood. Because these are learning experiences, their neural substrate likely involves memory, here affect-enhanced episodic memory. Inaugural object relations are encoded by the hippocampus-amygdala synaptic plasticity, and systems-consolidated by medial prefrontal cortex (mPFC). Self- and object-mental representations, extracted from these early experiences, are at first dichotomized by contradictory affects evoked by frustrating and rewarding interactions (“partial object relations”). Such affective dichotomization appears to be genetically hardwired the amygdala. Intrinsic propensity of mPFC to form schematic frameworks for episodic memories may pilot non-conscious integration of dichotomized mental representations in neonates and infants. With the emergence of working memory in toddlers, an activated self- and object-representation of a particular valence can be juxtaposed with its memorized opposites creating a balanced cognitive-affective frame (conscious “integration of object relations”). Specific events of object relations are forgotten but nevertheless profoundly influence the mental future of the individual, acting (i) as implicit schema-affect templates that regulate attentional priorities, relevance, and preferential assimilation of new information based on past experience, and (ii) as basic units of experience that are, under normal circumstances, integrated as attractors or “focal points” for interactive self-organization of functional brain networks that underlie the mind. A failure to achieve integrated object relations is predictive of poor adult emotional and social outcomes, including personality disorder. Cognitive, cellular-, and systems-neuroscience of episodic memory appear to support key postulates of object relations theory and help elucidate neural mechanisms of psychodynamic psychotherapy. Derived through the dual prism of psychoanalysis and neuroscience, the gained insights may offer new directions to enhance mental health and improve treatment of multiple forms of psychopathology.

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Mixing memory and desire: How memory reactivation supports deliberative decision‐making

Wang

Feng

Bornstein

2021

WIRES Cognitive Science

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Memories affect nearly every aspect of our mental life. They allow us to both resolve uncertainty in the present and to construct plans for the future. Recently, renewed interest in the role memory plays in adaptive behavior has led to new theoretical advances and empirical observations. We review key findings, with particular emphasis on how the retrieval of many kinds of memories affect deliberative action selection. These results are interpreted in a sequential inference framework, in which reinstatements from memory serve as "samples" of potential action outcomes. The resulting model suggests a central role for the dynamics of memory reactivation in determining the influence of different kinds of memory in decisions. We propose that representation-specific dynamics can implement a bottom-up "product of experts" rule that integrates multiple sets of action-outcome predictions weighted on the basis of their uncertainty. We close by reviewing related findings and identifying areas for further research.

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Hippocampal remapping as hidden state inference

Cited by 121 publications

References 113 publications

How many neurons are sufficient for perception of cortical activity?

How many neurons are sufficient for perception of cortical activity?

Neuroscience of Object Relations in Health and Disorder: A Proposal for an Integrative Model

Mixing memory and desire: How memory reactivation supports deliberative decision‐making

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