Dataset Information

A Distributed Neural Code in the Dentate Gyrus and in CA1.

ABSTRACT: Neurons are often considered specialized functional units that encode a single variable. However, many neurons are observed to respond to a mix of disparate sensory, cognitive, and behavioral variables. For such representations, information is distributed across multiple neurons. Here we find this distributed code in the dentate gyrus and CA1 subregions of the hippocampus. Using calcium imaging in freely moving mice, we decoded an animal's position, direction of motion, and speed from the activity of hundreds of cells. The response properties of individual neurons were only partially predictive of their importance for encoding position. Non-place cells encoded position and contributed to position encoding when combined with other cells. Indeed, disrupting the correlations between neural activities decreased decoding performance, mostly in CA1. Our analysis indicates that population methods rather than classical analyses based on single-cell response properties may more accurately characterize the neural code in the hippocampus.

SUBMITTER: Stefanini F

PROVIDER: S-EPMC7442694 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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A Distributed Neural Code in the Dentate Gyrus and in CA1.

Stefanini Fabio F Kushnir Lyudmila L Jimenez Jessica C JC Jennings Joshua H JH Woods Nicholas I NI Stuber Garret D GD Kheirbek Mazen A MA Hen René R Fusi Stefano S

Neuron 20200609 4

Neurons are often considered specialized functional units that encode a single variable. However, many neurons are observed to respond to a mix of disparate sensory, cognitive, and behavioral variables. For such representations, information is distributed across multiple neurons. Here we find this distributed code in the dentate gyrus and CA1 subregions of the hippocampus. Using calcium imaging in freely moving mice, we decoded an animal's position, direction of motion, and speed from the activi ...[more]

PMID: 32521223

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Project description:BackgroundPathophysiological evidence from temporal lobe epilepsy models highlights the hippocampus as the most affected structure due to its high degree of neuroplasticity and control of the dynamics of limbic structures, which are necessary to encode information, conferring to it an intrinsic epileptogenicity. A loss in this control results in observable oscillatory perturbations called fast ripples, in epileptic rats those events are found in CA1, CA3, and the dentate gyrus (DG), which are the principal regions of the trisynaptic circuit of the hippocampus. The present work used Granger causality to address which relationships among these three regions of the trisynaptic circuit are needed to cause fast ripples in CA1 in an in vivo model. For these purposes, male Wistar rats (210-300 g) were injected with a single dose of pilocarpine hydrochloride (2.4 mg/2 µl) into the right lateral ventricle and video-monitored 24 h/day to detect spontaneous and recurrent seizures. Once detected, rats were implanted with microelectrodes in these regions (fixed-recording tungsten wire electrodes, 60-μm outer diameter) ipsilateral to the pilocarpine injection. A total of 336 fast ripples were recorded and probabilistically characterized, from those fast ripples we made a subset of all the fast ripple events associated with sharp-waves in CA1 region (n = 40) to analyze them with Granger Causality.ResultsOur results support existing evidence in vitro in which fast ripple events in CA1 are initiated by CA3 multiunit activity and describe a general synchronization in the theta band across the three regions analyzed DG, CA3, and CA1, just before the fast ripple event in CA1 have begun.ConclusionThis in vivo study highlights the causal participation of the CA3 back-projection to the DG, a connection commonly overlooked in the trisynaptic circuit, as a facilitator of a closed-loop among these regions that prolongs the excitatory activity of CA3. We speculate that the loss of inhibitory drive of DG and the mechanisms of ripple-related memory consolidation in which also the CA3 back-projection to DG has a fundamental role might be underlying processes of the fast ripples generation in CA1.

Dataset Information

A Distributed Neural Code in the Dentate Gyrus and in CA1.

Publications

A Distributed Neural Code in the Dentate Gyrus and in CA1.

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