Optogenetic reduction of theta oscillations reveals that a single reliable time cell sequence is not required for working memory

Yong, Hyun Choong; Chang, HaoRan; Brandon, Mark P.

doi:10.1101/2022.06.25.497592

Cited by 4 publications

(1 citation statement)

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“…A major motivation for examining splitters is that it is an access point into internally generated activity during encoding, because all sensory cues at the time are identical. Time cells are similar to splitter cells in the sense that they show a large internally generated component, especially when sensory input is ‘clamped’ by running on a treadmill ( Kraus et al, 2013 ; MacDonald et al, 2011 ; Pastalkova et al, 2008 ; Yong et al, 2022 ). Note that "Flickering" between multiple maps or reference frames ( Jackson and Redish, 2007 ; Jezek et al, 2011 ; Kelemen and Fenton, 2010 ) and theta sequences ( Foster and Wilson, 2007 ; Skaggs et al, 1996 ) similarly are not sensory-driven.…”

Section: Introductionmentioning

confidence: 99%

Temporal context and latent state inference in the hippocampal splitter signal

Duvelle

Grieves

Meer

2023

eLife

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The hippocampus is thought to enable the encoding and retrieval of ongoing experience, the organization of that experience into structured representations like contexts, maps, and schemas, and the use of these structures to plan for the future. A central goal is to understand what the core computations supporting these functions are, and how these computations are realized in the collective action of single neurons. A potential access point into this issue is provided by ‘splitter cells’, hippocampal neurons that fire differentially on the overlapping segment of trajectories that differ in their past and/or future. However, the literature on splitter cells has been fragmented and confusing, owing to differences in terminology, behavioral tasks, and analysis methods across studies. In this review, we synthesize consistent findings from this literature, establish a common set of terms, and translate between single-cell and ensemble perspectives. Most importantly, we examine the combined findings through the lens of two major theoretical ideas about hippocampal function: representation of temporal context and latent state inference. We find that unique signature properties of each of these models are necessary to account for the data, but neither theory, by itself, explains all of its features. Specifically, the temporal gradedness of the splitter signal is strong support for temporal context, but is hard to explain using state models, while its flexibility and task-dependence is naturally accounted for using state inference, but poses a challenge otherwise. These theories suggest a number of avenues for future work, and we believe their application to splitter cells is a timely and informative domain for testing and refining theoretical ideas about hippocampal function.

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Section: Introductionmentioning

confidence: 99%

Temporal context and latent state inference in the hippocampal splitter signal

Duvelle

Grieves

Meer

2023

eLife

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Temporal encoding in deep reinforcement learning agents

Lin,

Huang,

Richards

2023

Sci Rep

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Neuroscientists have observed both cells in the brain that fire at specific points in time, known as “time cells”, and cells whose activity steadily increases or decreases over time, known as “ramping cells”. It is speculated that time and ramping cells support temporal computations in the brain and carry mnemonic information. However, due to the limitations in animal experiments, it is difficult to determine how these cells really contribute to behavior. Here, we show that time cells and ramping cells naturally emerge in the recurrent neural networks of deep reinforcement learning models performing simulated interval timing and working memory tasks, which have learned to estimate expected rewards in the future. We show that these cells do indeed carry information about time and items stored in working memory, but they contribute to behavior in large part by providing a dynamic representation on which policy can be computed. Moreover, the information that they do carry depends on both the task demands and the variables provided to the models. Our results suggest that time cells and ramping cells could contribute to temporal and mnemonic calculations, but the way in which they do so may be complex and unintuitive to human observers.

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Hierarchical Gradients of Encoded Spatial and Sensory Information in the Neocortex Are Attenuated by Dorsal Hippocampal Lesions

Demchuk,

Esteves,

Chang

et al. 2024

J. Neurosci.

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During navigation, the neocortex must actively integrate learned spatial context with current sensory experience to guide behaviours. However, the relative encoding of spatial and sensorimotor information among cortical cells, and whether hippocampal feedback continues to modify these properties in familiar environments, remains poorly understood. Thus, two-photon microscopy of male and female Thy1-GCaMP6s mice was used to longitudinally image neurons spanning superficial retrosplenial cortex and layers II-Va of primary and secondary motor cortices before and after bilateral dorsal hippocampal lesions. During behaviour on a familiar cued treadmill, the locations of two added obstacles were interchanged to decouple place-tuning from cue-tuning among the position correlated cells with fields at those locations. The subpopulations of place- and cue-tuned cells each formed interareal gradients such that higher-level cortical regions exhibited higher fractions of place cells, whereas lower-level regions exhibited higher fractions of cue cells. Position correlated cells in motor cortex also formed translaminar gradients; cells closer to the cortical surface were more likely to exhibit fields and were more sparsely and precisely tuned than deeper cells. After dorsal hippocampal lesions, a neural representation of the learned environment persisted but retrosplenial cortex exhibited significantly increased cue-tuning and, in motor cortices, both position correlated cell recruitment and population activity at the unstable obstacle locations became more homogeneously elevated across laminae. Altogether, these results support that the hippocampus continues to modulate cortical responses in familiar environments, and the relative impact of top-down feedback obeys hierarchical interareal and interlaminar gradients opposite to the flow of bottom-up sensory inputs.Significance statementDuring learning, the hippocampus imparts spatial context to memory representations throughout the superficial neocortex. However, the post-learning role of the hippocampus has not been well defined. The results of this study suggest that, during navigation of a familiar environment, the hippocampus continues to link unreliable sensory attributes to a stable contextual framework, effectively updating the learned model of the environment. The results are also consistent with top-down suppression of sensory-evoked activity during behaviour, which varied in strength according to hierarchical proximity to the hippocampus. This effect was abolished by bilateral lesions of the dorsal hippocampus, supporting that the hippocampus plays an ongoing role in propagating context-dependent predictions throughout the cortical hierarchy, a core hypothesis of the predictive coding theoretical framework.

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Optogenetic reduction of theta oscillations reveals that a single reliable time cell sequence is not required for working memory

Cited by 4 publications

References 54 publications

Temporal context and latent state inference in the hippocampal splitter signal

Temporal context and latent state inference in the hippocampal splitter signal

Temporal encoding in deep reinforcement learning agents

Hierarchical Gradients of Encoded Spatial and Sensory Information in the Neocortex Are Attenuated by Dorsal Hippocampal Lesions

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