Flexible theta sequence compression mediated via phase precessing interneurons

Chadwick, Angus; Rossum, Mark C. W. van; Nolan, Matthew F.

doi:10.7554/elife.20349

Cited by 28 publications

(45 citation statements)

References 78 publications

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“…spontaneously) and under naturalistic conditions (here self-paced, goal-directed navigation); these dynamics were moreover seen in the absence of overtly deliberative behaviors such as directed head scans (vicarious trial-and-error 12 ). Most immediately, these various properties suggest revised or new models of network-level theta dynamics [61][62][63][64][65][66] .…”

Section: Discussionmentioning

confidence: 99%

Regular cycling between representations of alternatives in the hippocampus

Kay

Sosa

et al. 2019

Preprint

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Cognitive faculties such as imagination, planning, and decision-making entail the ability to project into the future. Crucially, animal behavior in natural settings implies that the brain can generate representations of future scenarios not only quickly but also constantly over time, as external events continually unfold. Despite this insight, how the brain accomplishes this remains unknown. Here we report neural activity in the hippocampus encoding two future scenarios (two upcoming maze paths) in constant alternation at 8 Hz: one scenario per 8 Hz cycle (125 ms). We further found that the underlying cycling dynamic generalized across multiple hippocampal representations (location and direction) relevant to future behavior. These findings identify an extremely fast and regular dynamical process capable of representing future possibilities.

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Section: Discussionmentioning

confidence: 99%

Regular cycling between representations of alternatives in the hippocampus

Kay

Sosa

et al. 2019

Preprint

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“…There are several ongoing efforts along these lines (see review in Colgin (2013) ), but as emphasized by Colgin (2013) it is important to know what the underlying causes of theta generation are in the first place. In future work, for example, one might consider how our modeling work could be expanded and linked to functional theta modeling studies such as recent efforts by ( Chadwick et al, 2016 ) to capture the flexibility of theta sequences by including phase precessing interneurons in septo-hippocampal circuitry.…”

Section: Discussionmentioning

confidence: 99%

Combining theory, model and experiment to understand how theta rhythms are generated in the hippocampus

Ferguson

Chatzikalymniou

Skinner

2017

Preprint

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Scientists have observed theta rhythms (3–12 Hz) in the hippocampus for decades, but we do not have a clear understanding of how they are generated. This is largely due to the complex, multi-scale and nonlinear nature of the brain. To obtain insight into mechanisms underlying the generation of theta rhythms, we develop cellular-based network models of the hippocampus based on a whole hippocampus in vitro preparation that spontaneously generates theta rhythms. Building on theoretical and computational analyses, we find that spike frequency adaptation and post-inhibitory rebound constitute a basis for theta generation in large, minimally connected CA1 pyramidal (PYR) cell network models with fast-firing parvalbumin-positive (PV+) inhibitory cells. The particular theta frequency is more controlled by PYR to PV+ cell interactions rather than PV+ to PYR cell ones. We identify two scenarios by which theta rhythms can emerge and they can be differentiated by the ratio of excitatory to inhibitory currents to PV+ cells, but not to PYR cells. Only one of the scenarios is consistent with data from the whole hippocampus preparation, which leads to the prediction that the connection probability from PV+ to PYR cells needs to be larger than from PYR to PV+ cells. Our models can serve as a platform on which to build and develop an understanding of in vivo theta generation, and of microcircuit dynamics in the hippocampus.SignificanceBrain rhythms have been linked to cognition and are disrupted in disease. This makes it essential to understand mechanisms underlying their generation. Theory and mathematical models help provide an understanding and generate hypotheses. Together with experiment they contribute a framework to dissect the cellular contributions to network activity. However, models are inherently biological approximations, and thus the specific experimental and theoretical context upon which they are built will shape their output. If the approximations and contexts are not taken into account, particularly when using previously constructed models, misinterpretations can arise. Here, we use both theory and microcircuit models derived from a specific experimental context to provide insight into cellular-based mechanisms involved in theta rhythm generation in the hippocampus.

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“…In particular, phase precession of action potentials relative to the network theta rhythm (Fig. 1c) leads to the emergence of population level spike sequences that may be structured to support associative memory storage [18][19][20][21] . We will consider how synaptic integrative mechanisms may contribute to temporal codes that are linked to theta activity and that may be important for episodic memory.…”

Section: Take Down Policymentioning

confidence: 99%

“…Several classes of model include components implemented by active integration mechanisms (e.g. 21,105,[126][127][128] ). For example, ion channels that mediate spike frequency adaptation promote symmetry of firing in models in which phase precession involves asymmetric ramp-like synaptic inputs 10,127,129,130 .…”

Section: Theta Phase Precession and Theta Sequencesmentioning

confidence: 99%

“…Because numerous models generate phase precession, an approach to evaluate model predictions may be to also consider dependence of spatial codes on factors in addition to location 131 . In this spirit, a recent model suggests integrative properties may be tuned to account for dorsoventral differences in theta phase, and to maintain phase precession when running speed varies 21 . While experiments with knockout mice show that HCN1 channels are not required for either theta oscillations or for phase precession 51,101,132 , identifying which ion channels do play roles in phase precession may provide targets for testing contributions of theta sequences to spatial memory.…”

Section: Theta Phase Precession and Theta Sequencesmentioning

confidence: 99%

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Synaptic integrative mechanisms for spatial cognition

Schmidt-Hieber¹,

Nolan²

2017

Nat Neurosci

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Synaptic integrative mechanisms have profound effects on electrical signaling in the brain that, although largely hidden from recording methods that observe the spiking activity of neurons, may be critical for the encoding, storage and retrieval of information. Here we review roles for synaptic integrative mechanisms in the selection, generation and plasticity of place and grid fields, and in related temporal codes for the representation of space. We outline outstanding questions and challenges in the testing of hypothesized models for spatial computation and memory.

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Flexible theta sequence compression mediated via phase precessing interneurons

Cited by 28 publications

References 78 publications

Regular cycling between representations of alternatives in the hippocampus

Regular cycling between representations of alternatives in the hippocampus

Combining theory, model and experiment to understand how theta rhythms are generated in the hippocampus

Synaptic integrative mechanisms for spatial cognition

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