scholarly journals Modeling unitary fields and the single-neuron contribution to local field potentials in the hippocampus

2019 ◽  
Author(s):  
Maria Teleńczuk ◽  
Bartosz Teleńczuk ◽  
Alain Destexhe
Keyword(s):  
Local Field ◽  
Computational Models ◽  
Pyramidal Neurons ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Inhibitory Synapses ◽  
Simple Method ◽  
Hippocampal Pyramidal Neurons

AbstractSynaptic currents represent a major contribution to the local field potential (LFP) in brain tissue, but the respective contribution of excitatory and inhibitory synapses is not known. Here, we provide estimates of this contribution by using computational models of hippocampal pyramidal neurons, constrained by in vitro recordings. We focus on the unitary LFP (uLFP) generated by single neurons in the CA3 region of the hippocampus. We first reproduce experimental results for hippocampal basket cells, and in particular how inhibitory uLFP are distributed within hippocampal layers. Next, we calculate the uLFP generated by pyramidal neurons, using morphologically-reconstructed CA3 pyramidal cells. The model shows that the excitatory uLFP is of small amplitude, smaller than inhibitory uLFPs. Indeed, when the two are simulated together, inhibitory uLFPs mask excitatory uLFPs, which might create the illusion that the inhibitory field is generated by pyramidal cells. These results provide an explanation for the observation that excitatory and inhibitory uLFPs are of the same polarity, in vivo and in vitro. These results also show that somatic inhibitory currents are large contributors of the LFP, which is important information to interpret this signal. Finally, the results of our model might form the basis of a simple method to compute the LFP, which could be applied to point neurons for each cell type, thus providing a simple biologically-grounded method to calculate LFPs from neural networks.

Differential Impact of Miniature Synaptic Potentials on the Soma and Dendrites of Pyramidal Neurons In Vivo

1997 ◽  
Vol 78 (3) ◽  
pp. 1735-1739 ◽  
Author(s):  
Denis Paré ◽  
Elen Lebel ◽  
Eric J. Lang
Keyword(s):  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Input Resistance ◽  
Differential Impact ◽  
Synaptic Potentials ◽  
Ampa Antagonists ◽  
Intact Brain ◽  
The Impact

Paré, Denis, Elen LeBel, and Eric J. Lang. Differential impact of miniature synaptic potentials on the somata and dendrites of pyramidal neurons in vivo. J. Neurophysiol. 78: 1735–1739, 1997. We studied the impact of transmitter release resistant to tetrodotoxin (TTX) in morphologically identified neocortical pyramidal neurons recorded intracellularly in barbiturate-anesthetized cats. It was observed that TTX-resistant release occurs in pyramidal neurons in vivo and at much higher frequencies than was previously reported in vitro. Further, in agreement with previous findings indicating that GABAergic and glutamatergic synapses are differentially distributed in the somata and dendrites of pyramidal cells, we found that most miniature synaptic potentials were sensitive to γ-aminobutyric acid-A (GABAA) or α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) antagonists in presumed somatic and dendritic impalements, respectively. Pharmacological blockage of spontaneous synaptic events produced large increases in input resistance that were more important in dendritic (≈50%) than somatic (≈10%) impalements. These findings imply that in the intact brain, pyramidal neurons are submitted to an intense spike-independent synaptic bombardment that decreases the space constant of the cells. These results should be taken into account when extrapolating in vitro findings to intact brains.

Fiberoptic System for Recording Dendritic Calcium Signals in Layer 5 Neocortical Pyramidal Cells in Freely Moving Rats

2007 ◽  
Vol 98 (3) ◽  
pp. 1791-1805 ◽  
Author(s):  
Masanori Murayama ◽  
Enrique Pérez-Garci ◽  
Hans-Rudolf Lüscher ◽  
Matthew E. Larkum
Keyword(s):  
Pyramidal Neurons ◽  
Calcium Influx ◽  
Signal To Noise Ratio ◽  
Pyramidal Cells ◽  
Cellular Mechanisms ◽  
Novel Approach ◽  
Specific Loading ◽  
Apical Dendrites

Calcium influx into the dendritic tufts of layer 5 neocortical pyramidal neurons modifies a number of important cellular mechanisms. It can trigger local synaptic plasticity and switch the firing properties from regular to burst firing. Due to methodological limitations, our knowledge about Ca2+ spikes in the dendritic tuft stems mostly from in vitro experiments. However, it has been speculated that regenerative Ca2+ events in the distal dendrites correlate with distinct behavioral states. Therefore it would be most desirable to be able to record these Ca2+ events in vivo, preferably in the behaving animal. Here, we present a novel approach for recording Ca2+ signals in the dendrites of populations of layer 5 pyramidal neurons in vivo, which ensures that all recorded fluorescence changes are due to intracellular Ca2+ signals in the apical dendrites. The method has two main features: 1) bolus loading of layer 5 with a membrane-permeant Ca2+ dye resulting in specific loading of pyramidal cell dendrites in the upper layers and 2) a fiberoptic cable attached to a gradient index lens and a prism reflecting light horizontally at 90° to the angle of the apical dendrites. We demonstrate that the in vivo signal-to-noise ratio recorded with this relatively inexpensive and easy-to-implement fiberoptic-based device is comparable to conventional camera-based imaging systems used in vitro. In addition, the device is flexible and lightweight and can be used for recording Ca2+ signals in the distal dendritic tuft of freely behaving animals.

scholarly journals Transient oxytocin signaling primes the development and function of excitatory hippocampal neurons

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Silvia Ripamonti ◽  
Mateusz C Ambrozkiewicz ◽  
Francesca Guzzi ◽  
Marta Gravati ◽  
Gerardo Biella ◽  
...  
Keyword(s):  
Hippocampal Neurons ◽  
Pyramidal Neurons ◽  
Hippocampal Pyramidal Neurons ◽  
Excitatory Transmission ◽  
Oxytocin Receptors ◽  
Synapse Density ◽  
Protein Components ◽  
And Function

Beyond its role in parturition and lactation, oxytocin influences higher brain processes that control social behavior of mammals, and perturbed oxytocin signaling has been linked to the pathogenesis of several psychiatric disorders. However, it is still largely unknown how oxytocin exactly regulates neuronal function. We show that early, transient oxytocin exposure in vitro inhibits the development of hippocampal glutamatergic neurons, leading to reduced dendrite complexity, synapse density, and excitatory transmission, while sparing GABAergic neurons. Conversely, genetic elimination of oxytocin receptors increases the expression of protein components of excitatory synapses and excitatory synaptic transmission in vitro. In vivo, oxytocin-receptor-deficient hippocampal pyramidal neurons develop more complex dendrites, which leads to increased spine number and reduced γ-oscillations. These results indicate that oxytocin controls the development of hippocampal excitatory neurons and contributes to the maintenance of a physiological excitation/inhibition balance, whose disruption can cause neurobehavioral disturbances.

scholarly journals Defective Excitatory/Inhibitory Synaptic Balance and Increased Neuron Apoptosis in a Zebrafish Model of Dravet Syndrome

Cells ◽  
2019 ◽  
Vol 8 (10) ◽  
pp. 1199 ◽  
Author(s):  
Alexandre Brenet ◽  
Rahma Hassan-Abdi ◽  
Julie Somkhit ◽  
Constantin Yanicostas ◽  
Nadia Soussi-Yanicostas
Keyword(s):  
Local Field ◽  
Local Field Potential ◽  
Field Potential ◽  
Dravet Syndrome ◽  
Inhibitory Synapses ◽  
Neuron Activity ◽  
Loss Of Function ◽  
Zebrafish Model ◽  
Neuron Apoptosis

Dravet syndrome is a type of severe childhood epilepsy that responds poorly to current anti-epileptic drugs. In recent years, zebrafish disease models with Scn1Lab sodium channel deficiency have been generated to seek novel anti-epileptic drug candidates, some of which are currently undergoing clinical trials. However, the spectrum of neuronal deficits observed following Scn1Lab depletion in zebrafish larvae has not yet been fully explored. To fill this gap and gain a better understanding of the mechanisms underlying neuron hyperexcitation in Scn1Lab-depleted larvae, we analyzed neuron activity in vivo using combined local field potential recording and transient calcium uptake imaging, studied the distribution of excitatory and inhibitory synapses and neurons as well as investigated neuron apoptosis. We found that Scn1Lab-depleted larvae displayed recurrent epileptiform seizure events, associating massive synchronous calcium uptakes and ictal-like local field potential bursts. Scn1Lab-depletion also caused a dramatic shift in the neuronal and synaptic balance toward excitation and increased neuronal death. Our results thus provide in vivo evidence suggesting that Scn1Lab loss of function causes neuron hyperexcitation as the result of disturbed synaptic balance and increased neuronal apoptosis.

scholarly journals Defective excitatory/inhibitory synaptic balance and increased neuron apoptosis in a zebrafish model of Dravet syndrome

2019 ◽  
Author(s):  
Alexandre Brenet ◽  
Rahma Hassan-Abdi ◽  
Julie Somkhit ◽  
Constantin Yanicostas ◽  
Nadia Soussi-Yanicostas
Keyword(s):  
Local Field ◽  
Local Field Potential ◽  
Field Potential ◽  
Dravet Syndrome ◽  
Inhibitory Synapses ◽  
Neuron Activity ◽  
Loss Of Function ◽  
Zebrafish Model ◽  
Neuron Apoptosis

AbstractDravet syndrome is a type of severe childhood epilepsy that responds poorly to current anti-epileptic drugs. In recent years, zebrafish disease models with Scn1Lab sodium channel deficiency have been generated to seek novel anti-epileptic drug candidates, some of which are currently undergoing clinical trials. However, the spectrum of neuronal deficits observed following Scn1Lab depletion in zebrafish larvae has not yet been fully explored. To fill this gap and gain a better understanding of the mechanisms underlying neuron hyperexcitation in Scn1Lab-depleted larvae, we analyzed neuron activity in vivo using combined local field potential recording and transient calcium uptake imaging, studied the distribution of excitatory and inhibitory synapses and neurons as well as investigated neuron apoptosis. We found that Scn1Lab-depleted larvae displayed recurrent epileptiform seizure events, associating massive synchronous calcium uptakes and ictal-like local field potential bursts. Scn1Lab-depletion also caused a dramatic shift in the neuronal and synaptic balance toward excitation and increased neuronal death. Our results thus provide in vivo evidence suggesting that Scn1Lab loss of function causes neuron hyperexcitation as the result of disturbed synaptic balance and increased neuronal apoptosis.

scholarly journals A kernel-based method to calculate local field potentials from networks of spiking neurons

2020 ◽  
Author(s):  
Bartosz Telenczuk ◽  
Maria Telenczuk ◽  
Alain Destexhe
Keyword(s):  
Local Field ◽  
Pyramidal Neurons ◽  
Field Potential ◽  
Point Of View ◽  
Spiking Neurons ◽  
Inhibitory Neurons ◽  
List Type ◽  
Synaptic Currents ◽  
Hippocampal Pyramidal Neurons ◽  
Low Pass

AbstractBackgroundThe local field potential (LFP) is usually calculated from current sources arising from transmembrane currents, in particular in asymmetric cellular morphologies such as pyramidal neurons.New methodHere, we adopt a different point of view and relate the spiking of neurons to the LFP through efferent synaptic connections and provide a method to calculate LFPs.ResultsWe show that the so-called unitary LFPs (uLFP) provide the key to such a calculation. We show experimental measurements and simulations of uLFPs in neocortex and hippocampus, for both excitatory and inhibitory neurons. We fit a “kernel” function to measurements of uLFPs, and we estimate its spatial and temporal spread by using simulations of morphologically detailed reconstructions of hippocampal pyramidal neurons. Assuming that LFPs are the sum of uLFPs generated by every neuron in the network, the LFP generated by excitatory and inhibitory neurons can be calculated by convolving the trains of action potentials with the kernels estimated from uLFPs. This provides a method to calculate the LFP from networks of spiking neurons, even for point neurons for which the LFP is not easily defined. We show examples of LFPs calculated from networks of point neurons and compare to the LFP calculated from synaptic currents.ConclusionsThe kernel-based method provides a practical way to calculate LFPs from networks of point neurons.HighlightsWe provide a method to estimate the LFP from spiking neuronsThis method is based on kernels, estimated from experimental dataWe show applications of this method to calculate the LFP from networks of spiking neuronsWe show that the kernel-based method is a low-pass filtered version of the LFP calculated from synaptic currents

In Vitro and In Vivo Recording of Local Field Potential Oscillations in Mouse Hippocampus

2012 ◽  
Vol 2 (3) ◽  
pp. 273-294 ◽  
Author(s):  
L.H. Forsyth ◽  
J. Witton ◽  
J.T. Brown ◽  
A.D. Randall ◽  
M.W. Jones
Keyword(s):  
Local Field ◽  
Local Field Potential ◽  
Field Potential ◽  
Potential Oscillations ◽  
Mouse Hippocampus

scholarly journals Deciphering the contribution of oriens-lacunosum/moleculare (OLM) cells to intrinsic theta rhythms using biophysical local field potential (LFP) models

2018 ◽  
Author(s):  
Alexandra P. Chatzikalymniou ◽  
Frances K. Skinner
Keyword(s):  
Local Field ◽  
Average Power ◽  
Local Field Potentials ◽  
Field Potential ◽  
Cell Types ◽  
Field Potentials ◽  
Biophysical Modeling ◽  
Different Cell Types

AbstractOscillations in local field potentials (LFPs) commonly occur and analyses of them fuel brain function hypotheses. An understanding of the cellular correlates and pathways affecting LFPs is needed but many overlapping pathways in vivo makes this difficult to achieve. A prevalent LFP rhythm in the hippocampus is ‘theta’ (3-12 Hz). Theta rhythms emerge intrinsically in an in vitro whole hippocampus preparation and thus can be produced by local interactions between interneurons and pyramidal (PYR) cells. Overlapping pathways are much reduced in this preparation making it possible to decipher the contribution of different cell types to LFP generation. We focus on oriens-lacunosum/moleculare (OLM) cells as a major class of interneurons in the hippocampus. They can influence PYR cells through two distinct pathways, (i) by direct inhibition of PYR cell distal dendrites, and (ii) by indirect disinhibition of PYR cell proximal dendrites by inhibiting bistratified cells (BiCs) that target them. We use previous inhibitory network models and build biophysical LFP models using volume conductor theory. We assess the effect of OLM cells to ongoing intrinsic LFP theta rhythms by directly comparing our model LFP features with experiment. We find that robust LFP theta responses adhering to reproducible experimental criteria occur only for particular connectivities between OLM cells and BiCs. Decomposition of the LFP reveals that OLM cell inputs onto the PYR cell regulate robustness of LFP responses without affecting average power and that the robust response depends on co-activation of distal inhibition and basal excitation. We use our models to estimate the spatial extent of the region generating LFP theta rhythms, leading us to predict that about 22,000 PYR cells participate in generating the LFP theta rhythm. Besides allowing us to understand OLM cells’ contributions to intrinsic theta rhythms, our work can drive hypothesis developments of cellular contributions in vivo.Author SummaryOscillatory local field potentials (LFPs) are extracellularly recorded potentials that are widely used to interpret information processing in the brain. For example, theta LFP rhythms (3-12 Hz) are correlated with memory processing and it is known that particular inhibitory cell types control their existence. As such, it is critical for us to appreciate how various cell types contribute to the characteristics of LFP rhythms. A precise biophysical modeling scheme linking activity at the cellular level and the recorded signal has been established. However, it is difficult to assess cellular contributions in vivo because of many spatiotemporally overlapping pathways that prevent the unambiguous separation of signals. Using an in vitro preparation that exhibits intrinsic theta (3-12 Hz) rhythms and where there is much less overlap, we build biophysical LFP models to explore cell contributions to ongoing intrinsic theta rhythms. We uncover distinct contributions from different cell types and show that robust theta rhythms depend specifically on one of the cell types. We are able to determine this because our LFP models have direct links with experiment and we are able to perform thousands of simulations.

scholarly journals Pyramidal Neurons Switch From Integrators In Vitro to Resonators Under In Vivo-Like Conditions

2008 ◽  
Vol 100 (6) ◽  
pp. 3030-3042 ◽  
Author(s):  
Steven A. Prescott ◽  
Stéphanie Ratté ◽  
Yves De Koninck ◽  
Terrence J. Sejnowski
Keyword(s):  
Pyramidal Neurons ◽  
Outward Current ◽  
Membrane Conductance ◽  
Pyramidal Cells ◽  
Oscillatory Behavior ◽  
Operating Conditions ◽  
Dynamical Analysis ◽  
Class 1

During wakefulness, pyramidal neurons in the intact brain are bombarded by synaptic input that causes tonic depolarization, increased membrane conductance (i.e., shunting), and noisy fluctuations in membrane potential; by comparison, pyramidal neurons in acute slices typically experience little background input. Such differences in operating conditions can compromise extrapolation of in vitro data to explain neuronal operation in vivo. For instance, pyramidal neurons have been identified as integrators (i.e., class 1 neurons according to Hodgkin's classification of intrinsic excitability) based on in vitro experiments but that classification is inconsistent with the ability of hippocampal pyramidal neurons to oscillate/resonate at theta frequency since intrinsic oscillatory behavior is limited to class 2 neurons. Using long depolarizing stimuli and dynamic clamp to reproduce in vivo-like conditions in slice experiments, we show that CA1 hippocampal pyramidal cells switch from integrators to resonators, i.e., from class 1 to class 2 excitability. The switch is explained by increased outward current contributed by the M-type potassium current IM, which shifts the balance of inward and outward currents active at perithreshold potentials and thereby converts the spike-initiating mechanism as predicted by dynamical analysis of our computational model. Perithreshold activation of IM is enhanced by the depolarizing shift in spike threshold caused by shunting and/or sodium channel inactivation secondary to tonic depolarization. Our conclusions were validated by multiple comparisons between simulation and experimental data. Thus even so-called “intrinsic” properties may differ qualitatively between in vitro and in vivo conditions.

scholarly journals Synaptic GABAA Activation Inhibits AMPA-Kainate Receptor–Mediated Bursting in the Newborn (P0–P2) Rat Hippocampus

2000 ◽  
Vol 83 (1) ◽  
pp. 359-366 ◽  
Author(s):  
Karri Lamsa ◽  
J. Matias Palva ◽  
Eva Ruusuvuori ◽  
Kai Kaila ◽  
Tomi Taira
Keyword(s):  
Pyramidal Neurons ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Neuronal Population ◽  
Excitatory Input ◽  
Calcium Oscillations ◽  
Rat Hippocampus ◽  
Network Activity ◽  
Ca1 Pyramidal Cells

The mechanisms of synaptic transmission in the rat hippocampus at birth are assumed to be fundamentally different from those found in the adult. It has been reported that in the CA3-CA1 pyramidal cells a conversion of “silent” glutamatergic synapses to conductive α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) synapses starts gradually after P2. Further, GABA via its depolarizing action seems to give rise to grossly synchronous yet slow calcium oscillations. Therefore, GABA is generally thought to have a purely excitatory rather than an inhibitory role during the first postnatal week. In the present study field potential recordings and gramicidin perforated and whole cell clamp techniques as well as K+-selective microelectrodes were used to examine the relative contributions of AMPA and GABAA receptors to network activity of CA3-CA1 pyramidal cells in the newborn rat hippocampus. As early as postnatal day( P 0–P2), highly coherent spontaneous firing of CA3 pyramidal cells was seen in vitro. Negative-going extracellular spikes confined to periodic bursts (interval 16 ± 3 s) consisting of 2.9 ± 0.1 spikes were observed in stratum pyramidale. The spikes were accompanied by AMPA-R–mediated postsynaptic currents (PSCs) in simultaneously recorded pyramidal neurons (7.6 ± 3.0 unitary currents per burst). In CA1 pyramidal cells synchronous discharging of CA3 circuitry produced a barrage of AMPA currents at >20 Hz frequencies, thus demonstrating a transfer of the fast CA3 network activity to CA1 area. Despite its depolarizing action, GABAA-R–mediated transmission appeared to exert inhibition in the CA3 pyramidal cell population. The GABAA-R antagonist bicuculline hypersynchronized the output of glutamatergic CA3 circuitry and increased the network-driven excitatory input to the pyramidal neurons, whereas the GABAA-R agonist muscimol (100 nM) did the opposite. However, the occurrence of unitary GABAA-R currents was increased after muscimol application from 0.66 ± 0.16 s−1 to 1.43 ± 0.29 s−1. It was concluded that AMPA synapses are critical in the generation of spontaneous high-frequency bursts in CA3 as well as in CA3-CA1 transmission as early as P0–P2 in rat hippocampus. Concurrently, although GABAA-R–mediated depolarization may excite hippocampal interneurons, in CA3 pyramidal neurons it can restrain excitatory inputs and limit the size of the activated neuronal population.

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