scholarly journals Heterogeneous Firing Responses Predict Diverse Couplings to Presynaptic Activity in mice Layer V Pyramidal Neurons

2016 ◽  
Author(s):  
Yann Zerlaut ◽  
Alain Destexhe
Keyword(s):  
Membrane Potential ◽  
Synaptic Input ◽  
Pyramidal Neurons ◽  
Network Activity ◽  
Local Network ◽  
Potential Fluctuations ◽  
Branching Rule ◽  
Layer V ◽  
Different Levels ◽  
Membrane Potential Fluctuations

In this study, we present a theoretical framework combining experimental characterizations and analytical calculus to capture the firing rate input-output properties of single neurons in the fluctuation-driven regime. Our framework consists of a two-step procedure to treat independently how the dendritic input translates into somatic fluctuation variables, and how the latter determine action potential firing. We use this framework to investigate the functional impact of the heterogeneity in firing responses found experimentally in young mice layer V pyramidal cells. We first design and calibrate in vitro a simplified morphological model of layer V pyramidal neurons with a dendritic tree following Rall's branching rule. Then, we propose an analytical derivation for the membrane potential fluctuations at the soma as a function of the properties of the synaptic input in dendrites. This mathematical description allows us to easily emulate various forms of synaptic input: either balanced, unbalanced, synchronized, purely proximal or purely distal synaptic activity. We find that those different forms of input activity lead to various impact on the membrane potential fluctuations properties, thus raising the possibility that individual neurons will differentially couple to specific forms of activity as a result of their different firing response. We indeed found such a heterogeneous coupling between synaptic input and firing response for all types of presynaptic activity. This heterogeneity can be explained by different levels of cellular excitability in the case of the balanced, unbalanced, synchronized and purely distal activity. A notable exception appears for proximal dendritic inputs: increasing the input level can either promote firing response in some cells, or suppress it in some other cells whatever their individual excitability. This behavior can be explained by different sensitivities to the speed of the fluctuations, which was previously associated to different levels of sodium channel inactivation and density. Because local network connectivity rather targets proximal dendrites, our results suggest that this aspect of biophysical heterogeneity might be relevant to neocortical processing by controlling how individual neurons couple to local network activity.

Spontaneous Subthreshold Membrane Potential Fluctuations and Action Potential Variability of Rat Corticostriatal and Striatal Neurons In Vivo

1997 ◽  
Vol 77 (4) ◽  
pp. 1697-1715 ◽  
Author(s):  
Edward A. Stern ◽  
Anthony E. Kincaid ◽  
Charles J. Wilson
Keyword(s):  
Membrane Potential ◽  
Synaptic Input ◽  
High Frequency ◽  
Action Potentials ◽  
State Transitions ◽  
Striatal Neurons ◽  
Interspike Intervals ◽  
Potential Fluctuations ◽  
Membrane Potential Fluctuations

Stern, Edward A., Anthony E. Kincaid, and Charles J. Wilson. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J. Neurophysiol. 77: 1697–1715, 1997. We measured the timing of spontaneous membrane potential fluctuations and action potentials of medial and lateral agranular corticostriatal and striatal neurons with the use of in vivo intracellular recordings in urethan-anesthetized rats. All neurons showed spontaneous subthreshold membrane potential shifts from 7 to 32 mV in amplitude, fluctuating between a hyperpolarized down state and depolarized up state. Action potentials arose only during the up state. The membrane potential state transitions showed a weak periodicity with a peak frequency near 1 Hz. The peak of the frequency spectra was broad in all neurons, indicating that the membrane potential fluctuations were not dominated by a single periodic function. At frequencies >1 Hz, the log of magnitude decreased linearly with the log of frequency in all neurons. No serial dependence was found for up and down state durations, or for the time between successive up or down state transitions, showing that the up and down state transitions are not due to superimposition of noisy inputs onto a single frequency. Monte Carlo simulations of stochastic synaptic inputs to a uniform finite cylinder showed that the Fourier spectra obtained for corticostriatal and striatal neurons are inconsistent with a Poisson-like synaptic input, demonstrating that the up state is not due to an increase in the strength of an unpatterned synaptic input. Frequency components arising from state transitions were separated from those arising from the smaller membrane potential fluctuations within each state. A larger proportion of the total signal was represented by the fluctuations within states, especially in the up state, than was predicted by the simulations. The individual state spectra did not correspond to those of random synaptic inputs, but reproduced the spectra of the up and down state transitions. This suggests that the process causing the state transitions and the process responsible for synaptic input may be the same. A high-frequency periodic component in the up states was found in the majority of the corticostriatal cells in the sample. The average size of the component was not different between neurons injected with QX-314 and control neurons. The high-frequency component was not seen in any of our sample of striatal cells. Corticostriatal and striatal neurons' coefficients of variation of interspike intervals ranged from 1.0 to 1.9. When interspike intervals including a down state were subtracted from the calculation, the coefficient of variation ranged from 0.4 to 1.1, indicating that a substantial proportion of spike interval variance was due to the subthreshold membrane potential fluctuations.

scholarly journals Direct Pathway Neurons in Mouse Dorsolateral Striatum In Vivo Receive Stronger Synaptic Input than Indirect Pathway Neurons

2019 ◽  
Author(s):  
Marko Filipović ◽  
Maya Ketzef ◽  
Ramon Reig ◽  
Ad Aertsen ◽  
Gilad Silberberg ◽  
...  
Keyword(s):  
Membrane Potential ◽  
Synaptic Input ◽  
Excitatory Input ◽  
Medium Spiny Neurons ◽  
Indirect Pathway ◽  
Potential Fluctuations ◽  
Direct Pathway ◽  
Spiny Neurons ◽  
Membrane Potential Fluctuations

AbstractStriatal projection neurons, the medium spiny neurons (MSNs), play a crucial role in various motor and cognitive functions. MSNs express either D1 or D2 type dopamine receptors and initiate the direct-pathway (dMSNs) or indirect pathways (iMSNs) of the basal ganglia, respectively. dMSNs have been shown to receive more inhibition than iMSNs from intrastriatal sources. Based on these findings, computational modelling of the striatal network has predicted that under healthy conditions dMSNs should receive more excitatory input than iMSNs. To test this prediction, we analyzed in vivo whole-cell recordings from dMSNs and iMSNs in healthy and dopamine-depleted (6OHDA) anaesthetized mice. By comparing their membrane potential fluctuations, we found that dMSNs exhibited considerably larger membrane potential fluctuations over a wide frequency range. Furthermore, by comparing the spike-triggered average membrane potentials, we found that dMSNs depolarized towards the spike threshold significantly faster than iMSNs did. Together, these finding corroborate the theoretical prediction that direct-pathway MSNs receive stronger input than indirect-pathway neurons. Finally, we found that dopamine-depleted mice exhibited no difference between the membrane potential fluctuations of dMSNs and iMSNs. These data provide new insights into the question how a lack of dopamine may lead to behavior deficits associated with Parkinson’s disease.Significance statementThe direct and indirect pathways of the basal ganglia originate from the D1 and D2 type dopamine receptor expressing medium spiny neurons (dMSNs and iMSNs), respectively. To understand the role of the striatum in brain function and dysfunction it is important to characterize the differences in synaptic inputs to the two MSN types. Theoretical results predicted that dMSNs should receive stronger excitatory input than iMSNs. Here, we studied membrane potential fluctuation statistics of MSNs recorded in vivo in anaesthetized mice and found that dMSNs, indeed, received stronger synaptic input than iMSNs. We corroborated this finding by spike-triggered membrane potential analysis, showing that dMSNs spiking required more synaptic input than iMSNs spiking did, as had been predicted by computational models.

Traits of criticality in membrane potential fluctuations of pyramidal neurons in the CA 1 region of rat hippocampus

2018 ◽  
Vol 48 (6) ◽  
pp. 2343-2353 ◽  
Author(s):  
Efstratios K. Kosmidis ◽  
Yiannis F. Contoyiannis ◽  
Costas Papatheodoropoulos ◽  
Fotios K. Diakonos
Keyword(s):  
Membrane Potential ◽  
Pyramidal Neurons ◽  
Rat Hippocampus ◽  
Potential Fluctuations ◽  
Membrane Potential Fluctuations

Membrane potential fluctuations produced by glutamate in nerve cells of the squid

1975 ◽  
Vol 191 (1105) ◽  
pp. 561-565 ◽  
Keyword(s):  
Membrane Potential ◽  
Neuromuscular Junctions ◽  
Noise Analysis ◽  
Postsynaptic Membrane ◽  
Nerve Cells ◽  
Voltage Fluctuations ◽  
Potential Fluctuations ◽  
Synaptic Inputs ◽  
Small Voltage ◽  
Membrane Potential Fluctuations

Glutamate-induced potential changes have been recorded with intracellular electrodes in nerve cells of the squid. The responses are accompanied by small voltage fluctuations which resemble postsynaptic ‘membrane noise’ observed at neuromuscular junctions. Certain limitations are discussed in extending the noise analysis to neurons with multiple synaptic inputs.

Action of barium and potassium ions on membrane potential fluctuations of rat papillary cardiomyocytes

1987 ◽  
Vol 103 (3) ◽  
pp. 283-286
Author(s):  
S. I. Zakharov ◽  
K. Yu. Bogdanov ◽  
A. V. Zaitsev ◽  
L. V. Rozenshtraukh
Keyword(s):  
Membrane Potential ◽  
Potassium Ions ◽  
Potential Fluctuations ◽  
Membrane Potential Fluctuations

scholarly journals IgSF11 homophilic adhesion proteins promote layer-specific synaptic assembly of the cortical interneuron subtype

2021 ◽  
Vol 7 (29) ◽  
pp. eabf1600
Author(s):  
Yasufumi Hayano ◽  
Yugo Ishino ◽  
Jung Ho Hyun ◽  
Carlos G. Orozco ◽  
André Steinecke ◽  
...  
Keyword(s):  
Molecular Mechanisms ◽  
Pyramidal Neurons ◽  
Cell Types ◽  
Network Activity ◽  
Local Network ◽  
Immunoglobulin Superfamily ◽  
Specific Cell ◽  
Loss Of Function ◽  
Adhesion Proteins ◽  
Homophilic Adhesion

The most prominent structural hallmark of the mammalian neocortical circuitry is the layer-based organization of specific cell types and synaptic inputs. Accordingly, cortical inhibitory interneurons (INs), which shape local network activity, exhibit subtype-specific laminar specificity of synaptic outputs. However, the underlying molecular mechanisms remain unknown. Here, we demonstrate that Immunoglobulin Superfamily member 11 (IgSF11) homophilic adhesion proteins are preferentially expressed in one of the most distinctive IN subtypes, namely, chandelier cells (ChCs) that specifically innervate axon initial segments of pyramidal neurons (PNs), and their synaptic laminar target. Loss-of-function experiments in either ChCs or postsynaptic cells revealed that IgSF11 is required for ChC synaptic development in the target layer. While overexpression of IgSF11 in ChCs enlarges ChC presynaptic boutons, expressing IgSF11 in nontarget layers induces ectopic ChC synapses. These findings provide evidence that synapse-promoting adhesion proteins, highly localized to synaptic partners, determine the layer-specific synaptic connectivity of the cortical IN subtype.

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