The Effect of Spatially Inhomogeneous Extracellular Electric Fields on Neurons

Anastassiou, Costas A.; Montgomery, Sean M.; Barahona, Mauricio; Buzsáki, György; Koch, Christof

doi:10.1523/jneurosci.3635-09.2010

Cited by 180 publications

(170 citation statements)

References 63 publications

(87 reference statements)

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“…First, similar to several previous studies (7,8), our model assumes a homogenous and resistive extracellular field in arriving at the local field potentials. Although biophysical and experimental studies point to nonresistive components and nonhomogeneities in the extracellular fields, the impacts of these nonhomogeneities and nonresistive components are largely confined to higher frequencies (54)(55)(56). From these analyses, it stands to reason that the resistive and homogeneity assumptions are not debilitating for the conclusions drawn in our study where the range of frequencies is much lower, in the theta range.…”

Section: Discussionmentioning

confidence: 59%

HCN channels enhance spike phase coherence and regulate the phase of spikes and LFPs in the theta-frequency range

Sinha

Narayanan

2015

Proc. Natl. Acad. Sci. U.S.A.

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What are the implications for the existence of subthreshold ion channels, their localization profiles, and plasticity on local field potentials (LFPs)? Here, we assessed the role of hyperpolarizationactivated cyclic-nucleotide-gated (HCN) channels in altering hippocampal theta-frequency LFPs and the associated spike phase. We presented spatiotemporally randomized, balanced theta-modulated excitatory and inhibitory inputs to somatically aligned, morphologically realistic pyramidal neuron models spread across a cylindrical neuropil. We computed LFPs from seven electrode sites and found that the insertion of an experimentally constrained HCN-conductance gradient into these neurons introduced a location-dependent lead in the LFP phase without significantly altering its amplitude. Further, neurons fired action potentials at a specific theta phase of the LFP, and the insertion of HCN channels introduced large lags in this spike phase and a striking enhancement in neuronal spike-phase coherence. Importantly, graded changes in either HCN conductance or its half-maximal activation voltage resulted in graded changes in LFP and spike phases. Our conclusions on the impact of HCN channels on LFPs and spike phase were invariant to changes in neuropil size, to morphological heterogeneity, to excitatory or inhibitory synaptic scaling, and to shifts in the onset phase of inhibitory inputs. Finally, we selectively abolished the inductive lead in the impedance phase introduced by HCN channels without altering neuronal excitability and found that this inductive phase lead contributed significantly to changes in LFP and spike phase. Our results uncover specific roles for HCN channels and their plasticity in phase-coding schemas and in the formation and dynamic reconfiguration of neuronal cell assemblies.L ocal field potentials (LFPs) have been largely believed to be a reflection of the synaptic drive that impinges on a neuron. In recent experimental and modeling studies, there has been a lot of debate on the source and spatial extent of LFPs (1-9). However, most of these studies have used neurons with passive dendrites in their models and/or have largely focused on the contribution of spike-generating conductances to LFPs (7,8,10,11). Despite the widely acknowledged regulatory roles of subthreshold-activated ion channels and their somatodendritic gradients in the physiology and pathophysiology of synapses and neurons (12-17), the implications for their existence on LFPs and neuronal spike phase have surprisingly remained unexplored. This lacuna in LFP analysis is especially striking because local and widespread plasticity of these channels has been observed across several physiological and pathological conditions, translating to putative roles for these channels in neural coding, homeostasis, disease etiology and remedies, learning, and memory (16,(18)(19)(20)(21)(22)(23).In this study, we focus on the role of hyperpolarization-activated cyclic nucleotide-gated (HCN) channels that mediate the h current (I h ) in regulating LFPs and ...

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Section: Discussionmentioning

confidence: 59%

HCN channels enhance spike phase coherence and regulate the phase of spikes and LFPs in the theta-frequency range

Sinha

Narayanan

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…2C,D, 3, 4C-H ). Thus, by reducing the trial-to-trial variability of oscillatory phase rapidly following fixation onset, field potentials can lead to greater spiketiming reliability and consequently improve signal propagation (Azouz and Gray, 1999;Anastassiou et al, 2010Anastassiou et al, , 2011Fröhlich and McCormick, 2010;Ozen et al, 2010), as well as influence synaptic strength (Lubenov and Siapas, 2008;Masquelier et al, 2009Masquelier et al, , 2011Deco et al, 2011). The alpha band spike-phase locking was the weakest and least frequent, allowing a greater bandwidth for putative spike-phase coding in this lower frequency range (Fell and Axmacher, 2011).…”

Section: Modulation Of Spike Probability By Field Potential Phasementioning

confidence: 99%

Saccades during Object Viewing Modulate Oscillatory Phase in the Superior Temporal Sulcus

et al. 2011

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Saccadic eye movements (SEMs) are the primary means of gating visual information in primates and strongly influence visual perception. The active exploration of the visual environment ("active vision") via SEMs produces suppression during saccades and enhancement afterward (i.e., during fixation) in occipital visual areas. In lateral temporal lobe visual areas, the influence, if any, of eye movements is less well understood, despite the necessity of these areas for forming coherent percepts of objects. The upper bank of the superior temporal sulcus (uSTS) is one such area whose sensitivity to SEMs is unknown. We therefore examined how saccades modulate local field potentials (LFPs) in the uSTS of macaque monkeys while they viewed face and nonface object stimuli. LFP phase concentration increased following fixation onset in the alpha (8 -14 Hz), beta (14 -30 Hz), and gamma (30 -60 Hz) bands and was distinct from the image-evoked response.

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“…4B) is far below the reported threshold for directly evoking action potentials in pharmacologically isolated cells (Radman et al 2009). This suggests network mechanisms are involved such as an elevation of spontaneous firing rate or a modulation of spike timing distributed across many cells (Anastassiou et al 2010;Radman et al 2007;Reato et al 2010).…”

Section: Discussionmentioning

confidence: 99%

Low-intensity electric fields induce two distinct response components in neocortical neuronal populations

Wolff

2014

Journal of Neurophysiology

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The Effect of Spatially Inhomogeneous Extracellular Electric Fields on Neurons

Cited by 180 publications

References 63 publications

HCN channels enhance spike phase coherence and regulate the phase of spikes and LFPs in the theta-frequency range

HCN channels enhance spike phase coherence and regulate the phase of spikes and LFPs in the theta-frequency range

Saccades during Object Viewing Modulate Oscillatory Phase in the Superior Temporal Sulcus

Low-intensity electric fields induce two distinct response components in neocortical neuronal populations

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