scholarly journals Shape analysis of gamma rhythm supports a superlinear inhibitory regime in an inhibition-stabilized network

2021 ◽  
Author(s):  
R Krishnakumaran ◽  
Mohammed Raees ◽  
Supratim Ray

AbstractVisual inspection of stimulus-induced gamma oscillations (30-70 Hz) often reveals a non-sinusoidal shape. Such distortions are a hallmark of non-linear systems and are also observed in mean-field models of gamma oscillations. A thorough characterization of the shape of the gamma cycle can therefore provide additional constraints on the operating regime of such models. However, the gamma waveform has not been quantitatively characterized, partially because the first harmonic of gamma, which arises because of the non-sinusoidal nature of the signal, is typically weak and gets masked due to a broadband increase in power related to spiking. To address this, we recorded spikes and local field potential (LFP) from the primary visual cortex (V1) of two awake female macaques while presenting full-field gratings or iso-luminant chromatic hues that produced huge gamma oscillations with prominent peaks at harmonic frequencies in the power spectra. We found that gamma and its first harmonic always maintained a specific phase relationship, resulting in a distinctive shape with a sharp trough and a shallow peak. Interestingly, a Wilson-Cowan (WC) model operating in an inhibition stabilized mode could replicate the findings, but only when the inhibitory population operated in the super-linear regime, as predicted recently. However, another recently developed model of gamma that operates in a linear regime driven by stochastic noise failed to produce salient harmonics or the observed shape. Our results impose additional constraints on models that generate gamma oscillations and their operating regimes.Significance StatementGamma rhythm is not sinusoidal. Understanding these distortions could provide clues about the cortical network that generates the rhythm. Here, we use harmonic phase analysis to describe these waveforms quantitatively, and show that the gamma rhythm in macaque V1, during the presentation of fullscreen plain-hues and achromatic-gratings, has a signature arch-shaped waveform, despite the variation in power and frequency reported earlier. We further demonstrate using population rate models that the non-sinusoidal waveform is dependent on the operating domain of the system generating it. Consequently, shape analysis provides additional constraints on cortical models and their operating regimes.

2021 ◽  
Vol 15 ◽  
Author(s):  
Yuchen Zhou ◽  
Alex Sheremet ◽  
Jack P. Kennedy ◽  
Nicholas M. DiCola ◽  
Carolina B. Maciel ◽  
...  

The hippocampal local field potential (LFP) exhibits a strong correlation with behavior. During rest, the theta rhythm is not prominent, but during active behavior, there are strong rhythms in the theta, theta harmonics, and gamma ranges. With increasing running velocity, theta, theta harmonics and gamma increase in power and in cross-frequency coupling, suggesting that neural entrainment is a direct consequence of the total excitatory input. While it is common to study the parametric range between the LFP and its complementing power spectra between deep rest and epochs of high running velocity, it is also possible to explore how the spectra degrades as the energy is completely quenched from the system. Specifically, it is unknown whether the 1/f slope is preserved as synaptic activity becomes diminished, as low frequencies are generated by large pools of neurons while higher frequencies comprise the activity of more local neuronal populations. To test this hypothesis, we examined rat LFPs recorded from the hippocampus and entorhinal cortex during barbiturate overdose euthanasia. Within the hippocampus, the initial stage entailed a quasi-stationary LFP state with a power-law feature in the power spectral density. In the second stage, there was a successive erosion of power from high- to low-frequencies in the second stage that continued until the only dominant remaining power was <20 Hz. This stage was followed by a rapid collapse of power spectrum toward the absolute electrothermal noise background. As the collapse of activity occurred later in hippocampus compared with medial entorhinal cortex, it suggests that the ability of a neural network to maintain the 1/f slope with decreasing energy is a function of general connectivity. Broadly, these data support the energy cascade theory where there is a cascade of energy from large cortical populations into smaller loops, such as those that supports the higher frequency gamma rhythm. As energy is pulled from the system, neural entrainment at gamma frequency (and higher) decline first. The larger loops, comprising a larger population, are fault-tolerant to a point capable of maintaining their activity before a final collapse.


2018 ◽  
Author(s):  
Zoltan Nadasdy ◽  
Ágoston Török ◽  
T. Peter Nguyen ◽  
Jason Y. Shen ◽  
Deborah E. Briggs ◽  
...  

AbstractThe entorhinal cortex plays a vital role in our spatial awareness. Much focus has been placed on the spatial activity of its individual neurons, which fire in a grid-like pattern across an environment1. On a population level, however, neurons in the entorhinal cortex also display coherent rhythmic activity known as local field potential. These local field oscillations have been shown to correlate with behavioural states but it remains unclear how these oscillations relate to spatial behaviour and the spatial firing pattern of individual neurons. To investigate this, we recorded entorhinal cortical neurons in the human brain during spatial memory tasks performed in virtual environments. We observed a spatial modulation of the phase of action potentials relative to the local field potentials. In addition, the spike phase modulation displayed correlation with the movement of the avatar, displayed discrete phase tuning at the cellular level, rotated phase between electrodes, and expressed spatially coherent phase maps that scaled with the virtual environment. Using surrogate data, we demonstrated that spike phase coherence is dependent on the spatial phase dynamics of gamma oscillations. We argue that the spatial coordination of spike generation with gamma rhythm underlies the emergence of grid cell activity in the entorhinal cortex. These results shed a new light on the intricate interlacing between the spiking activity of neurons and local field oscillations in the brain.


2013 ◽  
Vol 110 (6) ◽  
pp. 1333-1345 ◽  
Author(s):  
Iain Stitt ◽  
Edgar Galindo-Leon ◽  
Florian Pieper ◽  
Gerhard Engler ◽  
Andreas K. Engel

In the superior colliculus (SC), visual afferent inputs from various sources converge in a highly organized way such that all layers form topographically aligned representations of contralateral external space. Despite this anatomical organization, it remains unclear how the layer-specific termination of different visual input pathways is reflected in the nature of visual response properties and their distribution across layers. To uncover the physiological correlates underlying the laminar organization of the SC, we recorded multiunit and local field potential activity simultaneously from all layers with dual-shank multichannel linear probes. We found that the location of spatial receptive fields was strongly conserved across all visual responsive layers. There was a tendency for receptive field size to increase with depth in the SC, with superficial receptive fields significantly smaller than deep receptive fields. Additionally, superficial layers responded significantly faster than deeper layers to flash stimulation. In some recordings, flash-evoked responses were characterized by the presence of gamma oscillatory activity (40–60 Hz) in multiunit and field potential signals, which was strongest in retinorecipient layers. While SC neurons tended to respond only weakly to full-field drifting gratings, we observed very similar oscillatory responses to the offset of grating stimuli, suggesting gamma oscillations are produced following light offset. Oscillatory spiking activity was highly correlated between horizontally distributed neurons within these layers, with oscillations temporally locked to the stimulus. Together, visual response properties provide physiological evidence reflecting the laminar-specific termination of visual afferent pathways in the SC, most notably characterized by the oscillatory entrainment of superficial neurons.


2009 ◽  
Vol 21 (12) ◽  
pp. 3335-3362 ◽  
Author(s):  
Naoki Masuda

Selective attention is often accompanied by gamma oscillations in local field potentials and spike field coherence in brain areas related to visual, motor, and cognitive information processing. Gamma oscillations are implicated to play an important role in, for example, visual tasks including object search, shape perception, and speed detection. However, the mechanism by which gamma oscillations enhance cognitive and behavioral performance of attentive subjects is still elusive. Using feedforward fan-in networks composed of spiking neurons, we examine a possible role for gamma oscillations in selective attention and population rate coding of external stimuli. We implement the concept proposed by Fries ( 2005 ) that under dynamic stimuli, neural populations effectively communicate with each other only when there is a good phase relationship among associated gamma oscillations. We show that the downstream neural population selects a specific dynamic stimulus received by an upstream population and represents it by population rate coding. The encoded stimulus is the one for which gamma rhythm in the corresponding upstream population is resonant with the downstream gamma rhythm. The proposed role for gamma oscillations in stimulus selection is to enable top-down control, a neural version of time division multiple access used in communication engineering.


2020 ◽  
Author(s):  
Y. Zhou ◽  
A. Sheremet ◽  
J. P. Kennedy ◽  
Nicholas M. DiCola ◽  
Carolina B. Maciel ◽  
...  

AbstractThe hippocampal local field potential (LFP) exhibits a strong correlation with behavior. During rest, the theta rhythm is not prominent, but during active behavior, there are strong rhythms in the theta, theta harmonics, and gamma ranges. With increasing running velocity, theta, theta harmonics and gamma increase in power and in cross-frequency coupling, suggesting that neural entrainment is a direct consequence of the total excitatory input. While it is common to study the parametric range between the LFP and its complementing power spectra between deep rest and epochs of high running velocity, it is also possible to explore how the spectra degrades as the energy is completely quenched from the system. Specifically, it is unknown whether the 1/f slope is preserved as synaptic activity becomes diminished, as low frequencies are generated by large pools of neurons while higher frequencies comprise the activity of more local neuronal populations. To test this hypothesis, we examined rat LFPs recorded from the hippocampus and entorhinal cortex during barbiturate overdose euthanasia. Within the hippocampus, the initial stage entailed a quasi-stationary stage when the LFP spectrum exhibited power-law feature while the frequency components over 20 Hz exhibited a power decay with a similar decay rate. This stage was followed by a rapid collapse of power spectrum towards the absolute electrothermal noise background. As the collapse of activity occurred later in hippocampus compared with medial entorhinal cortex or visual cortex, it suggests that the ability of a neural network to maintain the 1/f slope with decreasing energy is a function of general connectivity. Broadly, these data support the energy cascade theory where there is a cascade of energy from large cortical populations into smaller loops, such as those that supports the higher frequency gamma rhythm. As energy is pulled from the system, neural entrainment at gamma frequency (and higher) decline first. The larger loops, comprising a larger population, are fault-tolerant to a point capable of maintaining their activity before a final collapse.


2018 ◽  
Vol 17 (6) ◽  
pp. 404-411 ◽  
Author(s):  
Syeda Mehpara Farhat ◽  
Touqeer Ahmed

Background: Aluminum (Al) causes neurodegeneration and its toxic effects on cholinergic system in the brain is well documented. However, it is unknown whether and how Al changes oscillation patterns, driven by the cholinergic system, in the hippocampus. Objective: We studied acute effects of Al on nicotinic acetylcholine receptors (nAChRs)-mediated modulation of persistent gamma oscillations in the hippocampus. Method: The field potential recording was done in CA3 area of acute hippocampal slices. Results: Carbachol-induced gamma oscillation peak power increased (1.32±0.09mV2/Hz, P<0.01) in control conditions (without Al) by application of 10µM nicotine as compared to baseline value normalized to 1. This nicotine-induced facilitation of gamma oscillation peak power was found to depend on non-α7 nAChRs. In slices with Al pre-incubation for three to four hours, gamma oscillation peak power was reduced (5.4±1.8mV2/Hz, P<0.05) and facilitatory effect of nicotine on gamma oscillation peak power was blocked as compared to the control (18.06±2.1mV2/Hz) or one hour Al pre-incubated slices (11.3±2.5mV2/Hz). Intriguingly wash-out, after three to four hours of Al incubation, failed to restore baseline oscillation power and its facilitation by nicotine as no difference was observed in gamma oscillation peak power between Al wash-out slices (3.4±1.1mV2/Hz) and slices without washout (3.6±0.9mV2/Hz). Conclusion: This study shows that at cellular level, exposure of hippocampal tissue to Al compromised nAChR-mediated facilitation of cholinergic hippocampal gamma oscillations. Longer in vitro Al exposure caused permanent changes in hippocampal oscillogenic circuitry and changed its sensitivity to nAChR-modulation. This study will help to understand the possible mechanism of cognitive decline induced by Al.


Author(s):  
Luis Enrique Arroyo-García ◽  
Arturo G. Isla ◽  
Yuniesky Andrade-Talavera ◽  
Hugo Balleza-Tapia ◽  
Raúl Loera-Valencia ◽  
...  

AbstractIn Alzheimer’s disease (AD) the accumulation of amyloid-β (Aβ) correlates with degradation of cognition-relevant gamma oscillations. The gamma rhythm relies on proper neuronal spike-gamma coupling, specifically of fast-spiking interneurons (FSN). Here we tested the hypothesis that decrease in gamma power and FSN synchrony precede amyloid plaque deposition and cognitive impairment in AppNL-G-F knock-in mice (AppNL-G-F). The aim of the study was to evaluate the amyloidogenic pathology progression in the novel AppNL-G-F mouse model using in vitro electrophysiological network analysis. Using patch clamp of FSNs and pyramidal cells (PCs) with simultaneous gamma oscillation recordings, we compared the activity of the hippocampal network of wild-type mice (WT) and the AppNL-G-F mice at four disease stages (1, 2, 4, and 6 months of age). We found a severe degradation of gamma oscillation power that is independent of, and precedes Aβ plaque formation, and the cognitive impairment reported previously in this animal model. The degradation correlates with increased Aβ1-42 concentration in the brain. Analysis on the cellular level showed an impaired spike-gamma coupling of FSN from 2 months of age that correlates with the degradation of gamma oscillations. From 6 months of age PC firing becomes desynchronized also, correlating with reports in the literature of robust Aβ plaque pathology and cognitive impairment in the AppNL-G-F mice. This study provides evidence that impaired FSN spike-gamma coupling is one of the earliest functional impairment caused by the amyloidogenic pathology progression likely is the main cause for the degradation of gamma oscillations and consequent cognitive impairment. Our data suggests that therapeutic approaches should be aimed at restoring normal FSN spike-gamma coupling and not just removal of Aβ.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Bin Wang ◽  
Chuanliang Han ◽  
Tian Wang ◽  
Weifeng Dai ◽  
Yang Li ◽  
...  

AbstractStimulus-dependence of gamma oscillations (GAMMA, 30–90 Hz) has not been fully understood, but it is important for revealing neural mechanisms and functions of GAMMA. Here, we recorded spiking activity (MUA) and the local field potential (LFP), driven by a variety of plaids (generated by two superimposed gratings orthogonal to each other and with different contrast combinations), in the primary visual cortex of anesthetized cats. We found two distinct narrow-band GAMMAs in the LFPs and a variety of response patterns to plaids. Similar to MUA, most response patterns showed that the second grating suppressed GAMMAs driven by the first one. However, there is only a weak site-by-site correlation between cross-orientation interactions in GAMMAs and those in MUAs. We developed a normalization model that could unify the response patterns of both GAMMAs and MUAs. Interestingly, compared with MUAs, the GAMMAs demonstrated a wider range of model parameters and more diverse response patterns to plaids. Further analysis revealed that normalization parameters for high GAMMA, but not those for low GAMMA, were significantly correlated with the discrepancy of spatial frequency between stimulus and sites’ preferences. Consistent with these findings, normalization parameters and diversity of high GAMMA exhibited a clear transition trend and region difference between area 17 to 18. Our results show that GAMMAs are also regulated in the form of normalization, but that the neural mechanisms for these normalizations might differ from those of spiking activity. Normalizations in different brain signals could be due to interactions of excitation and inhibitions at multiple stages in the visual system.


2014 ◽  
Vol 11 (95) ◽  
pp. 20140058 ◽  
Author(s):  
Kiyoshi Kotani ◽  
Ikuhiro Yamaguchi ◽  
Lui Yoshida ◽  
Yasuhiko Jimbo ◽  
G. Bard Ermentrout

Gamma oscillations of the local field potential are organized by collective dynamics of numerous neurons and have many functional roles in cognition and/or attention. To mathematically and physiologically analyse relationships between individual inhibitory neurons and macroscopic oscillations, we derive a modification of the theta model, which possesses voltage-dependent dynamics with appropriate synaptic interactions. Bifurcation analysis of the corresponding Fokker–Planck equation (FPE) enables us to consider how synaptic interactions organize collective oscillations. We also develop the adjoint method (infinitesimal phase resetting curve) for simultaneous equations consisting of ordinary differential equations representing synaptic dynamics and a partial differential equation for determining the probability distribution of the membrane potential. This method provides a macroscopic phase response function (PRF), which gives insights into how it is modulated by external perturbation or internal changes of parameters. We investigate the effects of synaptic time constants and shunting inhibition on these gamma oscillations. The sensitivity of rising and decaying time constants is analysed in the oscillatory parameter regions; we find that these sensitivities are not largely dependent on rate of synaptic coupling but, rather, on current and noise intensity. Analyses of shunting inhibition reveal that it can affect both promotion and elimination of gamma oscillations. When the macroscopic oscillation is far from the bifurcation, shunting promotes the gamma oscillations and the PRF becomes flatter as the reversal potential of the synapse increases, indicating the insensitivity of gamma oscillations to perturbations. By contrast, when the macroscopic oscillation is near the bifurcation, shunting eliminates gamma oscillations and a stable firing state appears. More interestingly, under appropriate balance of parameters, two branches of bifurcation are found in our analysis of the FPE. In this case, shunting inhibition can effect both promotion and elimination of the gamma oscillation depending only on the reversal potential.


2012 ◽  
Vol 108 (5) ◽  
pp. 1392-1402 ◽  
Author(s):  
Elsie Premereur ◽  
Wim Vanduffel ◽  
Pieter R. Roelfsema ◽  
Peter Janssen

Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.


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