Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons

Fransén, Erik; Alonso, Ángel; Dickson, Clayton T.; Magistretti, Jacopo; Hasselmo, Michael E.

doi:10.1002/hipo.10198

Cited by 130 publications

(165 citation statements)

References 57 publications

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“…In contrast, membrane potential oscillations involve cyclical changes in two voltage-sensitive currents (Dickson et al, 2000;Fransen et al, 2004): (1) the persistent sodium current, I(NaP), and (2) the hyperpolarization-activated cation current I(h). These currents cause subthreshold membrane potential oscillations that can influence spike timing, but they are changing constantly with voltage and do not provide an equilibrium state.…”

Section: Biophysical Differences From Membrane Potential Oscillation mentioning

confidence: 99%

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

2008

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ABSTRACT:This article presents a model of grid cell firing based on the intrinsic persistent firing shown experimentally in neurons of entorhinal cortex. In this model, the mechanism of persistent firing allows individual neurons to hold a stable baseline firing frequency. Depolarizing input from speed-modulated head direction cells transiently shifts the frequency of firing from baseline, resulting in a shift in spiking phase in proportion to the integral of velocity. The convergence of input from different persistent firing neurons causes spiking in a grid cell only when the persistent firing neurons are within similar phase ranges. This model effectively simulates the two-dimensional firing of grid cells in open field environments, as well as the properties of theta phase precession. This model provides an alternate implementation of oscillatory interference models. The persistent firing could also interact on a circuit level with rhythmic inhibition and neurons showing membrane potential oscillations to code position with spiking phase. These mechanisms could operate in parallel with computation of position from visual angle and distance of stimuli. In addition to simulating two-dimensional grid patterns, models of phase interference can account for context-dependent firing in other tasks. In network simulations of entorhinal cortex, hippocampus, and postsubiculum, the reset of phase effectively replicates context-dependent firing by entorhinal and hippocampal neurons during performance of a continuous spatial alternation task, a delayed spatial alternation task with running in a wheel during the delay period (Pastalkova et al., Science, 2008), and a hairpin maze task.

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Section: Biophysical Differences From Membrane Potential Oscillation mentioning

confidence: 99%

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

2008

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“…The membrane potential oscillations discussed earlier depend on the hyperpolarization-activated inward current (Ih) (Dickson et al, 2000;Fransen et al, 2004), which has been observed in several other cortical regions including the hippocampus (Magee, 1998) and the cerebellum (Raman and Bean, 1999). Activated by hyperpolarization, the I(h) channel conducts both Na 1 and K 1 ions (Pape 1996), and is also referred to as the HCN channel (hyperpolarization-activated cAMPregulated cation channel).…”

Section: The Hyperpolarization-activated Cation Currentmentioning

confidence: 99%

Computation by oscillations: Implications of experimental data for theoretical models of grid cells

2008

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ABSTRACT:Recordings in awake, behaving animals demonstrate that cells in medial entorhinal cortex (mEC) show ''grid cell'' firing activity when a rat explores an open environment. Intracellular recording in slices from different positions along the dorsal to ventral axis show differences in intrinsic properties such as subthreshold membrane potential oscillations (MPO), resonant frequency, and the presence of the hyperpolarization-activated cation current (h-current). The differences in intrinsic properties correlate with differences in grid cell spatial scale along the dorsal-ventral axis of mEC. Two sets of computational models have been proposed to explain the grid cell firing phenomena: oscillatory interference models and attractor-dynamic models. Both types of computational models are briefly reviewed, and cellular experimental evidence is interpreted and presented in the context of both models. The oscillatory interference model has variations that include an additive model and a multiplicative model. Experimental data on the voltage-dependence of oscillations presented here support the additive model. The additive model also simulates data from ventral neurons showing large spacing between grid firing fields within the limits of observed MPO frequencies. The interactions of h-current with synaptic modification suggest that the difference in intrinsic properties could also contribute to differences in grid cell properties due to attractor dynamics along the dorsal to ventral axis of mEC. Mechanisms of oscillatory interference and attractor dynamics may make complementary contributions to the properties of grid cell firing in entorhinal cortex. V

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“…The oscillatory dynamics emerge from the interaction between the persistent sodium current I NaP and the hyperpolarization activated inward current I h . The current descriptions are based on the data from [13,14]. The dynamics of I h are described by a single gating variable w(t) with activation function w ∞ (V ) and time constant τ w (V )/ϕ (in milliseconds).…”

Section: Subthreshold Oscillator Modelmentioning

confidence: 99%

“…Several ionic conductances can underlie these oscillations. In entorhinal cortex stellate cells, experiments have shown that the oscillations result from an interaction of the persistent sodium current I NaP and the hyperpolarization activated inward current I h [6,13,14]. Recordings from hippocampal CA1 pyramidal neurons have also demonstrated ongoing oscillations in the dendrites that include repetitive dendritic spikes, presumably involving Ca 2+ currents [15].…”

Section: Introductionmentioning

confidence: 99%

The role of ongoing dendritic oscillations in single-neuron dynamics

2009

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The dendritic tree contributes significantly to the elementary computations a neuron performs while converting its synaptic inputs into action potential output. Traditionally, these computations have been characterized as temporally local, near-instantaneous mappings from the current input of the cell to its current output, brought about by somatic summation of dendritic contributions that are generated in spatially localized functional compartments. However, recent evidence about the presence of oscillations in dendrites suggests a qualitatively different mode of operation: the instantaneous phase of such oscillations can depend on a long history of inputs, and under appropriate conditions, even dendritic oscillators that are remote may interact through synchronization. Here, we develop a mathematical framework to analyze the interactions of local dendritic oscillations, and the way these interactions influence single cell computations. Combining weakly coupled oscillator methods with cable theoretic arguments, we derive phase-locking states for multiple oscillating dendritic compartments. We characterize how the phase-locking properties depend on key parameters of the oscillating dendrite: the electrotonic properties of the (active) dendritic segment, and the intrinsic properties of the dendritic oscillators. As a direct consequence, we show how input to the dendrites can modulate phase-locking behavior and hence global dendritic coherence. In turn, dendritic coherence is able to gate the integration and propagation of synaptic signals to the soma, ultimately leading to an effective control of somatic spike generation. Our results suggest that dendritic oscillations enable the dendritic tree to operate on more global temporal and spatial scales than previously thought. 1 Author SummaryA central issue in biology is how do local sub-cellular processes result in global cellular consequences. For neurons this is especially relevant since these spatially extended cells convert local synaptic inputs into action potential output. The dendritic tree of a neuron, which is where most inputs arrive, expresses membrane conductances that can generate intrinsic nonlinearities. The distributions of these membrane conductances are typically highly nonuniform. The non-uniform distribution of membrane conductances can turn the dendritic tree into a network of sparsely spaced active "hot spots". A prominent phenomenon resulting from the dendritic nonlinearities are intrinsic membrane potential oscillations, which are typically recorded at the neuron's soma. Here we analyze whether the active local oscillatory "hot spots" can produce global membrane voltage oscillations. Our mathematical theory shows that indeed, even when local dendritic oscillators are coupled extremely weakly, they still lead to global oscillations. This global effect arises since the oscillators lock to each other. We then show how the biophysical parameters of the dendrites affect this global locking. It becomes clear that when the oscillators are sy...

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Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons

Cited by 130 publications

References 57 publications

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

Computation by oscillations: Implications of experimental data for theoretical models of grid cells

The role of ongoing dendritic oscillations in single-neuron dynamics

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