scholarly journals Defining the synaptic mechanisms that tune CA3-CA1 reactivation during sharp-wave ripples

2017 ◽  
Author(s):  
Paola Malerba ◽  
Matt W. Jones ◽  
Maxim A. Bazhenov
Keyword(s):  
Network Connectivity ◽  
Pyramidal Cells ◽  
Fine Tuning ◽  
Cell Pair ◽  
Sharp Wave ◽  
Sharp Waves ◽  
High Frequency Oscillations ◽  
Excitatory Activity ◽  
Hippocampal Network ◽  
Ca3 Pyramidal Cells

AbstractDuring non-REM sleep, memory consolidation is driven by a dialogue between hippocampus and cortex involving the reactivation of specific neural activity sequences (‘replay’). In the hippocampus, replay occurs during sharp-wave ripples (SWRs), short bouts of excitatory activity in area CA3 which induce high frequency oscillations in the inhibitory interneurons of area CA1. Despite growing evidence for the functional importance of replay, its neural mechanisms remain poorly understood. Here, we develop a novel theoretical model of hippocampal spiking during SWRs. In our model, noise-induced activation of CA3 pyramidal cells triggered an excitatory cascade capable of inducing local ripple events in CA1. Ripples occurred stochastically, with Schaffer Collaterals driving their coordination, so that localized sharp waves in CA3 produced consistently localized CA1 ripples. In agreement with experimental data, the majority of pyramidal cells in the model showed low reactivation probabilities across SWRs. We found, however, that a subpopulation of pyramidal cells had high reactivation probabilities, which derived from fine-tuning of the network connectivity. In particular, the excitatory inputs along synaptic pathway(s) converging onto cells and cell pairs controlled emergent single cell and cell pair reactivation, with inhibitory inputs and intrinsic cell excitability playing differential roles in CA3 vs. CA1. Our model predicts (1) that the hippocampal network structure driving the emergence of SWR is also able to generate and modulate reactivation, (2) inhibition plays a particularly prominent role in CA3 reactivation and (3) CA1 sequence reactivation is reliant on CA3-CA1 interactions rather than an intrinsic CA1 process.

scholarly journals Learning-induced sequence reactivation during sharp-wave ripples: a computational study

2017 ◽  
Author(s):  
Paola Malerba ◽  
Katya Tsimring ◽  
Maxim Bazhenov
Keyword(s):  
Computational Study ◽  
Activity Patterns ◽  
Pyramidal Cells ◽  
Learning Task ◽  
Network Activity ◽  
Sharp Wave ◽  
High Frequency Oscillations ◽  
Excitatory Activity ◽  
Hippocampal Network ◽  
Synaptic Changes

AbstractDuring sleep, memories formed during the day are consolidated in a dialogue between cortex and hippocampus. The reactivation of specific neural activity patterns – replay – during sleep has been observed in both structures and is hypothesized to represent a neuronal substrate of consolidation. In the hippocampus, replay happens during sharp wave – ripples (SWR), short bouts of excitatory activity in area CA3 which induce high frequency oscillations in area CA1. In particular, recordings of hippocampal cells which spike at a specific location (‘place cells’) show that recently learned trajectories are reactivated during SWR in the following sleep SWR. Despite the importance of sleep replay, its underlying neural mechanisms are still poorly understood.We developed a model of SWR activity, to study the effects of learning-induced synaptic changes on spontaneous sequence reactivation during SWR. The model implemented a paradigm including three epochs: Pre-sleep, learning and Post-sleep activity. We first tested the effects of learning on the hippocampal network activity through changes in a minimal number of synapses connecting selected pyramidal cells. We then introduced an explicit trajectory-learning task to the model, to obtain behavior-induced synaptic changes. The model revealed that the recently learned trajectory reactivates during sleep more often than other trajectories in the training field. The study predicts that the gain of reactivation rate during sleep following vs sleep preceding learning for a trained sequence of pyramidal cells depends on Pre-sleep activation of the same sequence, and on the amount of trajectory repetitions included in the training phase.

scholarly journals Premature changes in neuronal excitability account for hippocampal network impairment and autistic-like behavior in neonatal BTBR T+tf/J mice

2016 ◽  
Vol 6 (1) ◽  
Author(s):  
Giada Cellot ◽  
Laura Maggi ◽  
Maria Amalia Di Castro ◽  
Myriam Catalano ◽  
Rosanna Migliore ◽  
...  
Keyword(s):  
Neuronal Excitability ◽  
Single Channel ◽  
Pyramidal Cells ◽  
Inhibitory Effect ◽  
Neuronal Firing ◽  
Gabaergic Neurotransmission ◽  
Principal Cells ◽  
Hippocampal Network ◽  
Ca3 Pyramidal Cells ◽  
Experimental Findings

Abstract Coherent network oscillations (GDPs), generated in the immature hippocampus by the synergistic action of GABA and glutamate, both depolarizing and excitatory, play a key role in the construction of neuronal circuits. In particular, GDPs-associated calcium transients act as coincident detectors for enhancing synaptic efficacy at emerging GABAergic and glutamatergic synapses. Here, we show that, immediately after birth, in the CA3 hippocampal region of the BTBR T+tf/J mouse, an animal model of idiopathic autism, GDPs are severely impaired. This effect was associated with an increased GABAergic neurotransmission and a reduced neuronal excitability. In spite its depolarizing action on CA3 pyramidal cells (in single channel experiments E GABA was positive to E m ), GABA exerted at the network level an inhibitory effect as demonstrated by isoguvacine-induced reduction of neuronal firing. We implemented a computational model in which experimental findings could be interpreted as the result of two competing effects: a reduction of the intrinsic excitability of CA3 principal cells and a reduction of the shunting activity in GABAergic interneurons projecting to principal cells. It is therefore likely that premature changes in neuronal excitability within selective hippocampal circuits of BTBR mice lead to GDPs dysfunction and behavioral deficits reminiscent of those found in autistic patients.

scholarly journals High-frequency oscillations and replay in a two-population model of hippocampal region CA1

2021 ◽  
Author(s):  
Wilhelm Braun ◽  
Raoul-Martin Memmesheimer
Keyword(s):  
Pyramidal Cell ◽  
High Frequency ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Basket Cell ◽  
Hippocampal Region ◽  
Short Pulses ◽  
Sharp Wave ◽  
High Frequency Oscillations

Hippocampal sharp wave/ripple oscillations are a prominent pattern of collective activity, which consists of a strong overall increase of activity with onmodulated (140 − 200 Hz) ripple oscillations. Despite its prominence and its experimentally demonstrated importance for memory consolidation, the mechanisms underlying its generation are to date not understood. Several models assume that recurrent networks of inhibitory cells alone can explain the generation and main characteristics of the ripple oscillations. Recent experiments, however, indicate that in addition to inhibitory basket cells, the pattern requires in vivo the activity of the local population of excitatory pyramidal cells. Here we study a model for networks in the hippocampal region CA1 incorporating such a local excitatory population of pyramidal neurons and investigate its ability to generate ripple oscillations using extensive simulations. We find that with biologically plausible values for single neuron, synapse and connectivity parameters, random connectivity and absent strong feedforward drive to the inhibitory population, oscillation patterns similar to in vivo sharp wave/ripples can only be generated if excitatory cell spiking is triggered by short pulses of external excitation. Specifically, whereas temporally broad excitation can lead to high-frequency oscillations in the ripple range, sparse pyramidal cell activity is only obtained with pulse-like external CA3 excitation. Further simulations indicate that such short pulses could originate from dendritic spikes in the apical or basal dendrites of CA1 pyramidal cells, which are triggered by coincident spike arrivals from hippocampal region CA3. Finally we show that replay of sequences by pyramidal neurons and ripple oscillations can arise intrinsically in CA1 due to structured connectivity that gives rise to alternating excitatory pulse and inhibitory gap coding; the latter implies phases of silence in specific basket cell groups and selective disinhibition of groups of pyramidal neurons. This general mechanism for sequence generation leads to sparse pyramidal cell and dense basket cell spiking, does not rely on synfire chain-like feedforward excitation and may be relevant for other brain regions as well.

scholarly journals Disruption of perineuronal nets increases the frequency of sharp wave ripples

2017 ◽  
Author(s):  
ZhiYong Sun ◽  
P. Lorenzo Bozzelli ◽  
Adam Caccavano ◽  
Megan Allen ◽  
Jason Balmuth ◽  
...  
Keyword(s):  
Slow Wave Sleep ◽  
Neuronal Cell ◽  
Pyramidal Cells ◽  
Neuronal Population ◽  
Stratum Radiatum ◽  
Perineuronal Nets ◽  
Ca1 Pyramidal Cells ◽  
Sharp Wave ◽  
Initial Excitation ◽  
Ca3 Pyramidal Cells

AbstractHippocampal sharp wave ripples (SWRs) represent irregularly occurring synchronous neuronal population events that are observed during phases of rest and slow wave sleep. SWR activity that follows learning involves sequential replay of training-associated neuronal assemblies and is critical for systems level memory consolidation. SWRs are initiated by CA2 or CA3 pyramidal cells and require initial excitation of CA1 pyramidal cells as well as subsequent participation of parvalbumin (PV) expressing fast spiking (FS) inhibitory interneurons. These interneurons are relatively unique in that they represent the major neuronal cell type known to be surrounded by perineuronal nets (PNNs), lattice like structures composed of a hyaluronin backbone that surround the cell soma and proximal dendrites. Though the function of the PNN is not completely understood, previous studies suggest it may serve to localize glutamatergic input to synaptic contacts and thus influence the activity of ensheathed cells. Noting that FS PV interneurons impact the activity of pyramidal cells thought to initiate SWRs, and that their activity is critical to ripple expression, we examine the effects of PNN integrity on SWR activity in the hippocampus. Extracellular recordings from the stratum radiatum of 490 micron horizontal murine hippocampal hemisections demonstrate SWRs that occur spontaneously in CA1. As compared to vehicle, pretreatment (120 min) of paired hemislices with hyaluronidase, which cleaves the hyaluronin backbone of the PNN, decreases PNN integrity and increases SWR frequency. Pretreatment with chondroitinase, which cleaves PNN side chains, also increases SWR frequency. Together, these data contribute to an emerging appreciation of extracellular matrix as a regulator of neuronal plasticity and suggest that one function of mature perineuronal nets could be to modulate the frequency of SWR events.

scholarly journals Longitudinal changes in hippocampal network connectivity in Alzheimer's disease

2021 ◽  
Author(s):  
Sophie Dautricourt ◽  
Robin Flores ◽  
Brigitte Landeau ◽  
Géraldine Poisnel ◽  
Matthieu Vanhoutte ◽  
...  
Keyword(s):  
Alzheimer’S Disease ◽  
Alzheimer's Disease ◽  
Network Connectivity ◽  
Longitudinal Changes ◽  
Hippocampal Network

Postsynaptic hyperpolarization increases the strength of AMPA-mediated synaptic transmission at large synapses between mossy fibers and CA3 pyramidal cells

2000 ◽  
Vol 39 (12) ◽  
pp. 2288-2301 ◽  
Author(s):  
Nicola Berretta ◽  
Aleksej V Rossokhin ◽  
Alexander M Kasyanov ◽  
Maxim V Sokolov ◽  
Enrico Cherubini ◽  
...  
Keyword(s):  
Synaptic Transmission ◽  
Mossy Fibers ◽  
Pyramidal Cells ◽  
Ca3 Pyramidal Cells

scholarly journals A computational study of suppression of sharp wave ripple complexes by controlling calcium and gap junctions in pyramidal cells

Bioengineered ◽  
2021 ◽  
Vol 12 (1) ◽  
pp. 2603-2615
Author(s):  
Muhammad Mushtaq ◽  
Rizwan ul Haq ◽  
Waqas Anwar ◽  
Lisa Marshall ◽  
Maxim Bazhenov ◽  
...  
Keyword(s):  
Gap Junctions ◽  
Computational Study ◽  
Pyramidal Cells ◽  
Sharp Wave
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