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 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 Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output

2019 ◽  
Author(s):  
Matt Udakis ◽  
Victor Pedrosa ◽  
Sophie E.L. Chamberlain ◽  
Claudia Clopath ◽  
Jack R Mellor
Keyword(s):  
Pyramidal Neurons ◽  
Physiological Activity ◽  
Activity Patterns ◽  
Pyramidal Cells ◽  
Network Activity ◽  
Inhibitory Synapses ◽  
Ca1 Pyramidal Cells ◽  
Hippocampal Cell ◽  
Hippocampal Network

SummaryThe formation and maintenance of spatial representations within hippocampal cell assemblies is strongly dictated by patterns of inhibition from diverse interneuron populations. Although it is known that inhibitory synaptic strength is malleable, induction of long-term plasticity at distinct inhibitory synapses and its regulation of hippocampal network activity is not well understood. Here, we show that inhibitory synapses from parvalbumin and somatostatin expressing interneurons undergo long-term depression and potentiation respectively (PV-iLTD and SST-iLTP) during physiological activity patterns. Both forms of plasticity rely on T-type calcium channel activation to confer synapse specificity but otherwise employ distinct mechanisms. Since parvalbumin and somatostatin interneurons preferentially target perisomatic and distal dendritic regions respectively of CA1 pyramidal cells, PV-iLTD and SST-iLTP coordinate a reprioritisation of excitatory inputs from entorhinal cortex and CA3. Furthermore, circuit-level modelling reveals that PV-iLTD and SST-iLTP cooperate to stabilise place cells while facilitating representation of multiple unique environments within the hippocampal network.

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

Roles of Very Fast Ripple (500–1000Hz) in the Hippocampal Network During Status Epilepticus

2020 ◽  
pp. 2150002
Author(s):  
Jianmin Hao ◽  
Yan Cui ◽  
Bochao Niu ◽  
Liang Yu ◽  
Yuhang Lin ◽  
...  
Keyword(s):  
Status Epilepticus ◽  
Temporal Lobe ◽  
Phase Locking ◽  
Epileptic Seizures ◽  
Network Activity ◽  
Slow Oscillations ◽  
Functional Roles ◽  
High Frequency Oscillations ◽  
Epileptiform Discharges ◽  
Hippocampal Network

Very fast ripples (VFRs, 500–1000[Formula: see text]Hz) are considered more specific than high-frequency oscillations (80–500[Formula: see text]Hz) as biomarkers of epileptogenic zones. Although VFRs are frequent abnormal phenomena in epileptic seizures, their functional roles remain unclear. Here, we detected the VFRs in the hippocampal network and tracked their roles during status epilepticus (SE) in rats with pilocarpine-induced temporal lobe epilepsy (TLE). All regions in the hippocampal network exhibited VFRs in the baseline, preictal, ictal and postictal states, with the ictal state containing the most VFRs. Moreover, strong phase-locking couplings existed between VFRs and slow oscillations (1–12[Formula: see text]Hz) in the ictal and postictal states for all regions. Further investigation indicated that during VFRs, the build-up of slow oscillations in the ictal state began from the temporal lobe and then spread through the whole hippocampal network via two different pathways, which might be associated with the underlying propagation of epileptiform discharges in the hippocampal network. Overall, we provide a functional description of the emergence of VFRs in the hippocampal network during SE, and we also establish that VFRs may be the physiological representation of the pathological alterations in hippocampal network activity during SE in TLE.

β-Adrenergic modulation of spontaneous spatiotemporal activity patterns and synchrony in hyperexcitable hippocampal circuits

2012 ◽  
Vol 108 (2) ◽  
pp. 658-671 ◽  
Author(s):  
Anupam Hazra ◽  
Robert Rosenbaum ◽  
Bernhard Bodmann ◽  
Siyuan Cao ◽  
Krešimir Josić ◽  
...  
Keyword(s):  
Propagation Velocity ◽  
Activity Patterns ◽  
Pyramidal Cells ◽  
Network Activity ◽  
Neural Activation ◽  
Ca1 Pyramidal Cells ◽  
Spatiotemporal Characteristics ◽  
Adrenergic Modulation ◽  
Whole Cell Recordings

A description of healthy and pathological brain dynamics requires an understanding of spatiotemporal patterns of neural activity and characteristics of its propagation between interconnected circuits. However, the structure and modulation of the neural activation maps underlying these patterns and their propagation remain elusive. We investigated effects of β-adrenergic receptor (β-AR) stimulation on the spatiotemporal characteristics of emergent activity in rat hippocampal circuits. Synchronized epileptiform-like activity, such as interictal bursts (IBs) and ictal-like events (ILEs), were evoked by 4-aminopyridine (4-AP), and their dynamics were studied using a combination of electrophysiology and fast voltage-sensitive dye imaging. Dynamic characterization of the spontaneous IBs showed that they originated in dentate gyrus/CA3 border and propagated toward CA1. To determine how β-AR modulates spatiotemporal characteristics of the emergent IBs, we used the β-AR agonist isoproterenol (ISO). ISO significantly reduced the spatiotemporal extent and propagation velocity of the IBs and significantly altered network activity in the 1- to 20-Hz range. Dual whole cell recordings of the IBs in CA3/CA1 pyramidal cells and optical analysis of those regions showed that ISO application reduced interpyramidal and interregional synchrony during the IBs. In addition, ISO significantly reduced duration not only of the shorter duration IBs but also the prolonged ILEs in 4-AP. To test whether the decrease in ILE duration was model dependent, we used a different hyperexcitability model, zero magnesium (0 Mg2+). Prolonged ILEs were readily formed in 0 Mg2+, and addition of ISO significantly reduced their durations. Taken together, these novel results provide evidence that β-AR activation dynamically reshapes the spatiotemporal activity patterns in hyperexcitable circuits by altering network rhythmogenesis, propagation velocity, and intercellular/regional synchronization.

scholarly journals An in vivo Calcium Imaging Approach for the Identification of Cell-Type Specific Patterns in the Developing Cortex

2021 ◽  
Vol 15 ◽  
Author(s):  
Alicia Che ◽  
Natalia V. De Marco García
Keyword(s):  
Neuronal Activity ◽  
Neural Development ◽  
Activity Patterns ◽  
Pyramidal Cells ◽  
Network Activity ◽  
Neuronal Diversity ◽  
Neuronal Populations ◽  
Cranial Window ◽  
Developing Neurons

Neuronal activity profoundly shapes the maturation of developing neurons. However, technical limitations have hampered the ability to capture the progression of activity patterns in genetically defined neuronal populations. This task is particularly daunting given the substantial diversity of pyramidal cells and interneurons in the neocortex. A hallmark in the development of this neuronal diversity is the participation in network activity that regulates circuit assembly. Here, we describe detailed methodology on imaging neuronal cohorts longitudinally throughout postnatal stages in the mouse somatosensory cortex. To capture neuronal activity, we expressed the genetically encoded calcium sensor GCaMP6s in three distinct interneuron populations, the 5HT3aR-expressing layer 1 (L1) interneurons, SST interneurons, and VIP interneurons. We performed cranial window surgeries as early as postnatal day (P) 5 and imaged the same cohort of neurons in un-anesthetized mice from P6 to P36. This Longitudinal two-photon imaging preparation allows the activity of single neurons to be tracked throughout development as well as plasticity induced by sensory experience and learning, opening up avenues of research to answer fundamental questions in neural development in vivo.

scholarly journals Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices

2021 ◽  
Vol 15 ◽  
Author(s):  
Lucie Landeck ◽  
Martin E. Kaiser ◽  
Dimitri Hefter ◽  
Andreas Draguhn ◽  
Martin Both
Keyword(s):  
Hippocampal Slices ◽  
Behavioral Flexibility ◽  
Pyramidal Cells ◽  
Enriched Environment ◽  
Cognitive Behavioral ◽  
Network Activity ◽  
Inhibitory Neurons ◽  
Synaptic Inhibition ◽  
Dependent Manner ◽  
Sharp Wave

Behavioral flexibility depends on neuronal plasticity which forms and adapts the central nervous system in an experience-dependent manner. Thus, plasticity depends on interactions between the organism and its environment. A key experimental paradigm for studying this concept is the exposure of rodents to an enriched environment (EE), followed by studying differences to control animals kept under standard conditions (SC). While multiple changes induced by EE have been found at the cellular-molecular and cognitive-behavioral levels, little is known about EE-dependent alterations at the intermediate level of network activity. We, therefore, studied spontaneous network activity in hippocampal slices from mice which had previously experienced EE for 10–15 days. Compared to control animals from standard conditions (SC) and mice with enhanced motor activity (MC) we found several differences in sharp wave-ripple complexes (SPW-R), a memory-related activity pattern. Sharp wave amplitude, unit firing during sharp waves, and the number of superimposed ripple cycles were increased in tissue from the EE group. On the other hand, spiking precision with respect to the ripple oscillations was reduced. Recordings from single pyramidal cells revealed a reduction in synaptic inhibition during SPW-R together with a reduced inhibition-excitation ratio. The number of inhibitory neurons, including parvalbumin-positive interneurons, was unchanged. Altered activation or efficacy of synaptic inhibition may thus underlie changes in memory-related network activity patterns which, in turn, may be important for the cognitive-behavioral effects of EE exposure.

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