scholarly journals Single-cell membrane potential fluctuations evince network scale-freeness and quasicriticality

2018 ◽  
Author(s):  
James Kenneth Johnson ◽  
Nathaniel C Wright ◽  
Ji Xia ◽  
Ralf Wessel

What information single neurons receive about general neural circuit activity is a fundamental question for neuroscience. Somatic membrane potential fluctuations are driven by the convergence of synaptic inputs from a diverse cross-section of upstream neurons. Furthermore, neural activity is often scale-free implying that some measurements should be the same, whether taken at large or small scales. Together, convergence and scale-freeness support the hypothesis that single membrane potential recordings carry useful information about high-dimensional cortical activity. Conveniently, the theory of "critical branching networks" (a purported explanation for scale-freeness) provides testable predictions about scale-free measurements which are readily applied to membrane potential fluctuations. To investigate, we obtained whole-cell current clamp recordings of pyramidal neurons in visual cortex of turtles with unknown genders. We isolated fluctuations in membrane potential below the firing threshold and analyzed them by adapting the definition of "neuronal avalanches" (spurts of population spiking). The membrane potential fluctuations we analyzed were scale-free and consistent with critical branching. These findings recapitulated results from large-scale cortical population data obtained separately in complementary experiments using microelectrode arrays (previously published (Shew et al., 2015)). Simultaneously recorded single-unit local field potential did not provide a good match; demonstrating the specific utility of membrane potential. Modeling shows that estimation of dynamical network properties from neuronal inputs is most accurate when networks are structured as critical branching networks. In conclusion, these findings extend evidence for critical branching while also establishing subthreshold pyramidal neuron membrane potential fluctuations as an informative gauge of high-dimensional cortical population activity.

1997 ◽  
Vol 77 (4) ◽  
pp. 1697-1715 ◽  
Author(s):  
Edward A. Stern ◽  
Anthony E. Kincaid ◽  
Charles J. Wilson

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.


1975 ◽  
Vol 191 (1105) ◽  
pp. 561-565 ◽  

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.


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

2017 ◽  
Vol 118 (5) ◽  
pp. 2579-2591 ◽  
Author(s):  
Mahmood S. Hoseini ◽  
Jeff Pobst ◽  
Nathaniel Wright ◽  
Wesley Clawson ◽  
Woodrow Shew ◽  
...  

Bursts of oscillatory neural activity have been hypothesized to be a core mechanism by which remote brain regions can communicate. Such a hypothesis raises the question to what extent oscillations are coherent across spatially distant neural populations. To address this question, we obtained local field potential (LFP) and membrane potential recordings from the visual cortex of turtle in response to visual stimulation of the retina. The time-frequency analysis of these recordings revealed pronounced bursts of oscillatory neural activity and a large trial-to-trial variability in the spectral and temporal properties of the observed oscillations. First, local bursts of oscillations varied from trial to trial in both burst duration and peak frequency. Second, oscillations of a given recording site were not autocoherent; i.e., the phase did not progress linearly in time. Third, LFP oscillations at spatially separate locations within the visual cortex were more phase coherent in the presence of visual stimulation than during ongoing activity. In contrast, the membrane potential oscillations from pairs of simultaneously recorded pyramidal neurons showed smaller phase coherence, which did not change when switching from black screen to visual stimulation. In conclusion, neuronal oscillations at distant locations in visual cortex are coherent at the mesoscale of population activity, but coherence is largely absent at the microscale of the membrane potential of neurons. NEW & NOTEWORTHY Coherent oscillatory neural activity has long been hypothesized as a potential mechanism for communication across locations in the brain. In this study we confirm the existence of coherent oscillations at the mesoscale of integrated cortical population activity. However, at the microscopic level of neurons, we find no evidence for coherence among oscillatory membrane potential fluctuations. These results raise questions about the applicability of the communication through coherence hypothesis to the level of the membrane potential.


2011 ◽  
Vol 589 (17) ◽  
pp. 4365-4381 ◽  
Author(s):  
Jan M. Schulz ◽  
Toni L. Pitcher ◽  
Shakuntala Savanthrapadian ◽  
Jeffery R. Wickens ◽  
Manfred J. Oswald ◽  
...  

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