scholarly journals GABA-Glutamate supramammillary neurons control theta and gamma oscillations in the dentate gyrus during paradoxical (REM) sleep

2019 ◽  
Author(s):  
Francesca Billwiller ◽  
Laura Castillo ◽  
Heba Elseedy ◽  
Anton Ivanovich Ivanov ◽  
Jennyfer Scapula ◽  
...  
Keyword(s):  
Dentate Gyrus ◽  
Rem Sleep ◽  
Slow Wave Sleep ◽  
Granule Cells ◽  
Structural Connectivity ◽  
Gamma Oscillations ◽  
Network Activity ◽  
Projection Neurons ◽  
Theta Power ◽  
Gamma Power

AbstractSeveral studies suggest that neurons from the lateral region of the SuM (SuML) innervating the dorsal dentate gyrus (DG) display a dual GABAergic and glutamatergic transmission and are specifically activated during paradoxical (REM) sleep (PS). The objective of the present study is to fully characterize the anatomical, neurochemical and electrophysiological properties of the SuML-DG projection neurons and to determine how they control DG oscillations and neuronal activation during PS and other vigilance states. For this purpose, we combine structural connectivity techniques using neurotropic viral vectors (rabies virus, AAV), neurochemical anatomy (immunohistochemistry, in situ hybridization) and imaging (light, electron and confocal microscopy) with in vitro (patch clamp) and in vivo (LFP, EEG) optogenetic and electrophysiological recordings performed in transgenic VGLUT2-cre male mice. At the cellular level, we show that the SuML-DG neurons co-release GABA and glutamate on dentate granule cells and increase the activity of a subset of DG granule cells. At the network level, we show that activation of the SuML-DG pathway increases theta power and frequency during PS as well as gamma power during PS and waking in the DG. At the behavioral level, we show that the activation of this pathway does not change animal behavior during PS, induces awakening during slow wave sleep and increases motor activity during waking. These results suggest that the SuML-DG pathway is capable of supporting the increase of theta and gamma power in the DG observed during PS and plays an important modulatory role of DG network activity during this state.Significant statementAn increase of theta and gamma power in the dentate gyrus (DG) is an hallmark of paradoxical (REM) sleep (PS) and is suggested to promote learning and memory consolidation by synchronizing hippocampal networks and increasing its outputs to cortical targets. However the neuronal networks involved in such control of DG activity during PS are poorly understood. The present study identifies a population of GABA/Glutamate neurons in the lateral supramammllary nucleus (SuML) innervating the DG that could support such control during PS. Indeed, we show that activation of these SuML-DG projections increase theta power and frequency as well as gamma power in the DG specifically during PS and modulate activity of a subset of DG granule cells.

scholarly journals GABA–glutamate supramammillary neurons control theta and gamma oscillations in the dentate gyrus during paradoxical (REM) sleep

2020 ◽  
Vol 225 (9) ◽  
pp. 2643-2668 ◽  
Author(s):  
Francesca Billwiller ◽  
Laura Castillo ◽  
Heba Elseedy ◽  
Anton Ivanovich Ivanov ◽  
Jennyfer Scapula ◽  
...  
Keyword(s):  
Dentate Gyrus ◽  
Rem Sleep ◽  
Slow Wave Sleep ◽  
Granule Cells ◽  
Structural Connectivity ◽  
Gamma Oscillations ◽  
Network Activity ◽  
Projection Neurons ◽  
Gamma Power

AbstractSeveral studies suggest that neurons from the lateral region of the SuM (SuML) innervating the dorsal dentate gyrus (DG) display a dual GABAergic and glutamatergic transmission and are specifically activated during paradoxical (REM) sleep (PS). The objective of the present study is to characterize the anatomical, neurochemical and electrophysiological properties of the SuML-DG projection neurons and to determine how they control DG oscillations and neuronal activation during PS and other vigilance states. For this purpose, we combine structural connectivity techniques using neurotropic viral vectors (rabies virus, AAV), neurochemical anatomy (immunohistochemistry, in situ hybridization) and imaging (light, electron and confocal microscopy) with in vitro (patch clamp) and in vivo (LFP, EEG) optogenetic and electrophysiological recordings performed in transgenic VGLUT2-cre male mice. At the cellular level, we show that the SuML-DG neurons co-release GABA and glutamate on dentate granule cells and increase the activity of a subset of DG granule cells. At the network level, we show that activation of the SuML-DG pathway increases theta power and frequency during PS as well as gamma power during PS and waking in the DG. At the behavioral level, we show that the activation of this pathway does not change animal behavior during PS, induces awakening during slow wave sleep and increases motor activity during waking. These results suggest that the SuML-DG pathway is capable of supporting the increase of theta and gamma power in the DG observed during PS and plays an important modulatory role of DG network activity during this state.

scholarly journals Substance P Enhances NMDA Channel Function in Hippocampal Dentate Gyrus Granule Cells

1998 ◽  
Vol 80 (1) ◽  
pp. 113-119 ◽  
Author(s):  
David N. Lieberman ◽  
Istvan Mody
Keyword(s):  
Substance P ◽  
Dentate Gyrus ◽  
Granule Cells ◽  
Excitatory Amino Acid ◽  
Calcium Influx ◽  
Network Activity ◽  
Hippocampal Dentate Gyrus ◽  
Adult Rat ◽  
Channel Function ◽  
Nmda Channel

Lieberman, David N. and Istvan Mody. Substance P enhances NMDA channel function in hippocampal dentate gyrus granule cells. J. Neurophysiol. 80: 113–119, 1998. Substance P (SP)–containing afferents and the NK-1 tachykinin receptor to which SP binds are present in the dentate gyrus of the rat; however, direct actions of SP on principal cells have not been demonstrated in this brain region. We have examined the effect of SP on N-methyl-d-aspartate (NMDA) channels from acutely isolated dentate gyrus granule cells of adult rat hippocampus to assess the ability of SP to regulate glutamatergic input. SP produces a robust enhancement of single NMDA channel function that is mimicked by the NK-1–selective agonist Sar9, Met(O2)11-SP. The SP-induced prolongation of NMDA channel openings is prevented by the selective NK-1 receptor antagonist (+)-(2 S,3 S)-3-(2-methoxybenzylamino)-2-phenylpiperidine (CP-99,994). Calcium influx or activation of protein kinase C were not required for the SP-induced increase in NMDA channel open durations. The dramatic enhancement of excitatory amino acid–mediated excitability by SP places this neuropeptide in a key position to gate activation of hippocampal network activity.

Gamma Oscillations Index Sustained Attention in a Brief Vigilance Task

2021 ◽  
Vol 65 (1) ◽  
pp. 546-550
Author(s):  
Lorraine Borghetti ◽  
Megan B. Morris ◽  
L. Jack Rhodes ◽  
Ashley R. Haubert ◽  
Bella Z. Veksler
Keyword(s):  
Sustained Attention ◽  
Gamma Oscillations ◽  
Time On Task ◽  
Potential Candidate ◽  
Theta Power ◽  
High Performers ◽  
Beta Power ◽  
Study Results ◽  
Gamma Power ◽  
Compensatory Effort

Sustained attention is an essential behavior in life, but often leads to performance decrements with time. Computational accounts of sustained attention suggest this is due to brief disruptions in goal-directed processing, or microlapses. Decreases in gamma spectral power are a potential candidate for indexing microlapses and discriminating between low and high performers in sustained attention tasks, while increases in beta, alpha, and theta power are expected to exhibit compensatory effort to offset fatigue. The current study tests these hypotheses in a 10-minute Psychomotor Vigilance Test, a context that eliminates confounds with measuring gamma frequencies. 34 participants ( Mage = 22.60; SDage = 4.08) volunteered in the study. Results suggested frontal gamma power declined with time-on-task, indicating reduction in central cognition. Beta power increased with time-on-task, suggesting compensatory effort; however, alpha and theta power did not increase. Additionally, gamma power discriminated between low and high performers, potentially suggesting motivational differences between the groups.

scholarly journals Differential origin of the activation of dorsal and ventral dentate gyrus granule cells during paradoxical (REM) sleep in the rat

2016 ◽  
Vol 222 (3) ◽  
pp. 1495-1507 ◽  
Author(s):  
Francesca Billwiller ◽  
Leslie Renouard ◽  
Olivier Clement ◽  
Patrice Fort ◽  
Pierre-Hervé Luppi
Keyword(s):  
Dentate Gyrus ◽  
Rem Sleep ◽  
Granule Cells

scholarly journals High-gamma activity in the human hippocampus during inter-trial rest periods of a virtual navigation task

2018 ◽  
Author(s):  
Yi Pu ◽  
Brian R. Cornwell ◽  
Douglas Cheyne ◽  
Blake W. Johnson
Keyword(s):  
Gamma Oscillations ◽  
Gamma Activity ◽  
Training Set ◽  
Virtual Navigation ◽  
Navigation Task ◽  
Theta Power ◽  
Rest Periods ◽  
Synthetic Aperture Magnetometry ◽  
High Gamma ◽  
Gamma Power

AbstractIn rodents, hippocampal cell assemblies formed during learning of a navigation task are observed to re-emerge during resting (offline) periods, accompanied by high-frequency oscillations (HFOs). This phenomenon is believed to reflect mechanisms for strengthening newly-formed memory traces. Using magnetoencephalography recordings and a beamforming source location algorithm (synthetic aperture magnetometry), we investigated high-gamma (80 – 140 Hz) oscillations in the hippocampal region in 18 human participants during inter-trial rest periods in a virtual navigation task. We found right hippocampal gamma oscillations mirrored the pattern of theta power in the same region during navigation, varying as a function of environmental novelty. Gamma power during inter-trial rest periods was positively correlated with theta power during navigation in the first training set when the environment was new and predicted faster learning in the subsequent training set two where the environment became familiar. These findings provide evidence for human hippocampal reactivation accompanied by high-gamma activities immediately after learning and establish a link between hippocampal high-gamma activities and memory consolidation.

scholarly journals Dendritic inhibition differentially regulates excitability of dentate gyrus parvalbumin-expressing interneurons and granule cells

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Claudio Elgueta ◽  
Marlene Bartos
Keyword(s):  
Dentate Gyrus ◽  
Granule Cells ◽  
Network Activity ◽  
Global Network ◽  
Perforant Path ◽  
Input Output ◽  
Inhibitory Effects ◽  
Cell Modeling ◽  
Fast Spiking ◽  
Whole Cell Recordings

AbstractFast-spiking parvalbumin-expressing interneurons (PVIs) and granule cells (GCs) of the dentate gyrus receive layer-specific dendritic inhibition. Its impact on PVI and GC excitability is, however, unknown. By applying whole-cell recordings, GABA uncaging and single-cell-modeling, we show that proximal dendritic inhibition in PVIs is less efficient in lowering perforant path-mediated subthreshold depolarization than distal inhibition but both are highly efficient in silencing PVIs. These inhibitory effects can be explained by proximal shunting and distal strong hyperpolarizing inhibition. In contrast, GC proximal but not distal inhibition is the primary regulator of their excitability and recruitment. In GCs inhibition is hyperpolarizing along the entire somato-dendritic axis with similar strength. Thus, dendritic inhibition differentially controls input-output transformations in PVIs and GCs. Dendritic inhibition in PVIs is suited to balance PVI discharges in dependence on global network activity thereby providing strong and tuned perisomatic inhibition that contributes to the sparse representation of information in GC assemblies.

Theta-gamma coupling during REM sleep depends on breathing rate

SLEEP ◽  
2021 ◽  
Author(s):  
Maximilian Hammer ◽  
Chrysovalandis Schwale ◽  
Jurij Brankačk ◽  
Andreas Draguhn ◽  
Adriano B L Tort
Keyword(s):  
Rem Sleep ◽  
Large Scale ◽  
Brain Activity ◽  
Gamma Oscillations ◽  
Network Activity ◽  
Breathing Rate ◽  
Nasal Breathing ◽  
Rate Dependent ◽  
Temporal Coupling ◽  
Scale Integration

Abstract Temporal coupling between theta and gamma oscillations is a hallmark activity pattern of several cortical networks and becomes especially prominent during REM sleep. In a parallel approach, nasal breathing has been recently shown to generate phase-entrained network oscillations which also modulate gamma. Both slow rhythms (theta and respiration-entrained oscillations) have been suggested to aid large-scale integration but they differ in frequency, display low coherence, and modulate different gamma sub-bands. Respiration and theta are therefore believed to be largely independent. In the present work, however, we report an unexpected but robust relation between theta-gamma coupling and respiration in mice. Interestingly, this relation takes place not through the phase of individual respiration cycles, but through respiration rate: the strength of theta-gamma coupling exhibits an inverted V-shaped dependence on breathing rate, leading to maximal coupling at breathing frequencies of 4-6 Hz. Noteworthy, when subdividing sleep epochs into phasic and tonic REM patterns, we find that breathing differentially relates to theta-gamma coupling in each state, providing new evidence for their physiological distinctiveness. Altogether, our results reveal that breathing correlates with brain activity not only through phase-entrainment but also through rate-dependent relations with theta-gamma coupling. Thus, the link between respiration and other patterns of cortical network activity is more complex than previously assumed.

scholarly journals Granule cells in the infrapyramidal blade of the dentate gyrus are activated during paradoxical (REM) sleep hypersomnia but not during wakefulness: a study using TRAP mice

SLEEP ◽  
2021 ◽  
Author(s):  
Risa Yamazaki ◽  
Dianru Wang ◽  
Anna De Laet ◽  
Renato Maciel ◽  
Claudio Agnorelli ◽  
...  
Keyword(s):  
Dentate Gyrus ◽  
Rem Sleep ◽  
Granule Cells ◽  
Paradoxical Sleep ◽  
Ca1 Neurons ◽  
Memory Reactivation ◽  
Supramammillary Nucleus ◽  
First Time ◽  
Number Of Cells

Abstract Study Objectives Determine whether in the hippocampus and the supramammillary nucleus (SuM) the same neurons are reactivated when mice are exposed one week apart to two periods of wakefulness (W-W), paradoxical sleep rebound (PSR-PSR) or a period of W followed by a period of PSR (W-PSR) Methods We combined the innovative TRAP2 mice method in which neurons expressing cFos permanently express tdTomato after tamoxifen injection with cFos immunohistochemistry. Results We found out that a large number of tdTomato+ and cFos+ cells are localized in the dentate gyrus (DG) after PSR and W while CA1 and CA3 contained both types of neurons only after W. The number of cFos+ cells in the infrapyramidal but not the suprapyramidal blade of the DG was positively correlated with the amount of PS. In addition, we did not find double-labeled cells in the DG whatever the group of mice. In contrast, a high percentage of CA1 neurons were double-labeled in W-W mice. Finally, in the supramammillary nucleus, a large number of cells were double-labeled in W-W, PSR-PSR but not in W-PSR mice. Conclusions Altogether, our results are the first to show that different neurons are activated during W and PS in the supramammillary nucleus and the hippocampus. Further, we showed for the first time that granule cells of the infrapyramidal blade of the DG are activated during PS but not during W. Further experiments are now needed to determine whether these granule cells belong to memory engrams inducing memory reactivation during PS.

scholarly journals Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus

Hippocampus ◽  
2010 ◽  
Vol 22 (1) ◽  
pp. 106-116 ◽  
Author(s):  
Clay O. Lacefield ◽  
Vladimir Itskov ◽  
Thomas Reardon ◽  
René Hen ◽  
Joshua A. Gordon
Keyword(s):  
Dentate Gyrus ◽  
Granule Cells ◽  
Network Activity

scholarly journals Gamma rhythm communication between entorhinal cortex and dentate gyrus neuronal assemblies

Science ◽  
2021 ◽  
Vol 372 (6537) ◽  
pp. eabf3119
Author(s):  
Antonio Fernández-Ruiz ◽  
Azahara Oliva ◽  
Marisol Soula ◽  
Florbela Rocha-Almeida ◽  
Gergo A. Nagy ◽  
...  
Keyword(s):  
Dentate Gyrus ◽  
Granule Cells ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Relevant Information ◽  
Brain Regions ◽  
Spike Timing ◽  
Dependent Manner ◽  
Gamma Frequency ◽  
Gamma Rhythm

Gamma oscillations are thought to coordinate the spike timing of functionally specialized neuronal ensembles across brain regions. To test this hypothesis, we optogenetically perturbed gamma spike timing in the rat medial (MEC) and lateral (LEC) entorhinal cortices and found impairments in spatial and object learning tasks, respectively. MEC and LEC were synchronized with the hippocampal dentate gyrus through high- and low-gamma-frequency rhythms, respectively, and engaged either granule cells or mossy cells and CA3 pyramidal cells in a task-dependent manner. Gamma perturbation disrupted the learning-induced assembly organization of target neurons. Our findings imply that pathway-specific gamma oscillations route task-relevant information between distinct neuronal subpopulations in the entorhinal-hippocampal circuit. We hypothesize that interregional gamma-time-scale spike coordination is a mechanism of neuronal communication.

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