The Continuity of Context: A Role for the Hippocampus

Maurer, Andrew P.; Nadel, Lynn

doi:10.1016/j.tics.2020.12.007

Cited by 60 publications

(45 citation statements)

References 81 publications

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“…It should be appreciated that a single synaptic event can have rhythmic entrainment to both "theta" and "gamma" bands, challenging the heuristic of independence across rhythms. Instead, the dynamic patterns in the LFP are closely related to how the activity spatio-temporally evolves a reentrant network (Berg et al, 2019;Maurer and Nadel, 2021). While there is comfort in giving independence to specific patterns like theta and gamma, neurobiology makes no such distinction.…”

Section: Discussionmentioning

confidence: 99%

Spectrum Degradation of Hippocampal LFP During Euthanasia

Zhou

Sheremet

Kennedy

et al. 2021

Front. Syst. Neurosci.

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The hippocampal local field potential (LFP) exhibits a strong correlation with behavior. During rest, the theta rhythm is not prominent, but during active behavior, there are strong rhythms in the theta, theta harmonics, and gamma ranges. With increasing running velocity, theta, theta harmonics and gamma increase in power and in cross-frequency coupling, suggesting that neural entrainment is a direct consequence of the total excitatory input. While it is common to study the parametric range between the LFP and its complementing power spectra between deep rest and epochs of high running velocity, it is also possible to explore how the spectra degrades as the energy is completely quenched from the system. Specifically, it is unknown whether the 1/f slope is preserved as synaptic activity becomes diminished, as low frequencies are generated by large pools of neurons while higher frequencies comprise the activity of more local neuronal populations. To test this hypothesis, we examined rat LFPs recorded from the hippocampus and entorhinal cortex during barbiturate overdose euthanasia. Within the hippocampus, the initial stage entailed a quasi-stationary LFP state with a power-law feature in the power spectral density. In the second stage, there was a successive erosion of power from high- to low-frequencies in the second stage that continued until the only dominant remaining power was <20 Hz. This stage was followed by a rapid collapse of power spectrum toward the absolute electrothermal noise background. As the collapse of activity occurred later in hippocampus compared with medial entorhinal cortex, it suggests that the ability of a neural network to maintain the 1/f slope with decreasing energy is a function of general connectivity. Broadly, these data support the energy cascade theory where there is a cascade of energy from large cortical populations into smaller loops, such as those that supports the higher frequency gamma rhythm. As energy is pulled from the system, neural entrainment at gamma frequency (and higher) decline first. The larger loops, comprising a larger population, are fault-tolerant to a point capable of maintaining their activity before a final collapse.

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Section: Discussionmentioning

confidence: 99%

Spectrum Degradation of Hippocampal LFP During Euthanasia

Zhou

Sheremet

Kennedy

et al. 2021

Front. Syst. Neurosci.

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“…In keeping with this observation, recent comparisons of dorsal and ventral hippocampal lesions in the MWT have shown that while dorsal lesions impair precise localization of goal locations, ventral damage impairs coarse localization in the MWT [16-18]. In relation to cellular recruitment, it is anticipated that cells in the dorsal hippocampus are more likely to be recruited due to a greater number of small place fields that would be required to tesselate a space than those with large fields in ventral hippocampus [6, 7]. Indeed, multiple groups have found that place cells in the dorsal hippocampus have multiple fields in large environments [46-50].…”

Section: Discussionmentioning

confidence: 99%

“…Specifically, the dorsal region is said to be necessary for spatial navigation and memory, and the ventral region is important for emotional processing [2, 4]. An alternative view, largely informed by the observation that place field size increases from dorsal to ventral regions, posits instead that the hippocampal longitudinal axis varies in its granularity of representation, wherein spatial-temporal resolution of representation decreases along the axis, ventrally [5-7].…”

Section: Introductionmentioning

confidence: 99%

Behaviour-drivenArcexpression is greater in dorsal than ventral CA1 regardless of task or sex differences

Lee

McHugh

Morgan

et al. 2021

Preprint

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Evidence from genetic, behavioural, anatomical, and physiological study suggests that the hippocampus functionally differs across its longitudinal (dorsoventral or septotemporal) axis. Although, how to best characterize functional and representational differences in the hippocampus across its long axis remains unclear. While some suggest that the hippocampus can be divided into dorsal and ventral subregions that support distinct cognitive functions, others posit that these regions vary in their granularity of representation, wherein spatial-temporal resolution decreases in the ventral (temporal) direction. Importantly, the cognitive and granular hypotheses make distinct predictions on cellular recruitment dynamics under conditions when animals perform tasks with qualitatively different cognitive-behavioural demands. The cognitive function account implies that dorsal and ventral cellular recruitment differs depending on relevant behavioural demands, while the granularity account suggests similar recruitment dynamics regardless of the nature of the task performed. Here, we quantified cellular recruitment with the immediate early gene (IEG) Arc across the entire longitudinal CA1 axis in female and male rats performing spatial-and fear-guided memory tasks. Our results show that recruitment is greater in dorsal than ventral CA1 regardless of task or sex. This experimentum crucis leads to the strong inference that the granularity hypothesis for functional differences across the longitudinal axis in the rodent hippocampus is correct.

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“…In fact, forgetting irrelevant experiences might be an adaptive biological process (Hardt et al, 2013) and resonates with the idea that the brain should form compact memory representations that have the highest utility for behavior. Tackling the question of what counts as an event or experience, a common theme in neuroscience has been to posit that the brain segments continuous experience into representations of distinct neural states that transition at boundaries between events or shifts in context (for reviews, see e.g., Richmond & Zacks, 2017;Brunec et al, 2018;Shin & DuBrow, 2020;Bird, 2020;Maurer & Nadel, 2021), a process that might also happen retroactively, after experiences have been obtained (Clewett et al, 2019). This formation of segmented memory traces is thought to be driven by various factors, including inferred changes in the environment (DuBrow et al, 2017), prediction error signals elicited by reward outcomes (Rouhani et al, 2020) or discontinuities in the statistical structure of the environment (Gershman et al, 2014).…”

Section: Box 2 What Is Replayed?mentioning

confidence: 99%

Replay in minds and machines

Wittkuhn¹,

Chien²,

Hall-McMaster³

2021

Preprint

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Experience-related brain activity patterns have been found to reactivate during sleep, wakeful rest, and brief pauses from active behavior. In parallel, machine learning research has found that experience replay can lead to substantial performance improvements in artificial agents. Together, these lines of research have significantly expanded our understanding of the potential computational benefits replay may provide to biological and artificial agents alike. We provide an overview of findings in replay research from neuroscience and machine learning and summarize the computational benefits an agent can gain from replay that cannot be achieved through direct interactions with the world itself. These benefits include faster learning and data efficiency, less forgetting, prioritizing important experiences, as well as improved planning and generalization. In addition to the benefits of replay for improving an agent's decision-making policy, we highlight the less-well studied aspect of replay in representation learning, wherein replay could provide a mechanism to learn the structure and relevant aspects of the environment. Thus, replay might help the agent to build task-appropriate state representations.

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The Continuity of Context: A Role for the Hippocampus

Cited by 60 publications

References 81 publications

Spectrum Degradation of Hippocampal LFP During Euthanasia

Spectrum Degradation of Hippocampal LFP During Euthanasia

Behaviour-drivenArcexpression is greater in dorsal than ventral CA1 regardless of task or sex differences

Replay in minds and machines

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