Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons

1993 ◽  
Vol 70 (1) ◽  
pp. 144-157 ◽  
Author(s):  
R. Klink ◽  
A. Alonso
Keyword(s):  
Membrane Potential ◽  
Entorhinal Cortex ◽  
Inward Rectification ◽  
Voltage Level ◽  
Medial Entorhinal Cortex ◽  
Potential Oscillations ◽  
Subthreshold Oscillations ◽  
Outward Rectification ◽  
Ionic Mechanisms ◽  
Membrane Potential Oscillations

1. Layer II of the medial entorhinal cortex is composed of two electrophysiologically and morphologically distinct types of projection neurons: stellate cells (SCs), which are distinguished by rhythmic subthreshold oscillatory activity, and non-SCs. The ionic mechanisms underlying their differential electroresponsiveness, particularly in the subthreshold range of membrane potentials, were investigated in an "in vitro" slice preparation. 2. In both SCs and non-SCs, the apparent membrane input resistance was markedly voltage dependent, respectively decreasing or increasing at hyperpolarized or subthreshold depolarized potential levels. Thus the neurons displayed inward rectification in the hyperpolarizing and depolarizing range. 3. In the depolarizing range, inward rectification was blocked by tetrodotoxin (TTX, 1 microM) in both types of neurons and thus shown to depend on the presence of a persistent low-threshold Na+ conductance (gNap). However, in the presence of TTX, pronounced outward rectification became manifest in the subthreshold depolarizing range of membrane potentials (positive to -60 mV) in the SCs but not in the non-SCs. 4. The rhythmic subthreshold membrane potential oscillations that were present only in the SCs were abolished by TTX and not by Ca2+ conductance block with Cd2+ or Co2+. Subthreshold oscillations thus rely on the activation of voltage-gated Na+, and not Ca2+, conductances. The Ca2+ conductance block also had no effect on the subthreshold outward rectification. 5. Prominent time-dependent inward rectification in the hyperpolarizing range in the SCs persisted after Na(+)- and Ca2+ conductance block. This rectification was not affected by Ba2+ (1 mM), but was blocked by Cs+ (1-4 mM). Therefore, it is most probably generated by a hyperpolarization-activated cationic current (Q-like current). However, the Q-like current appears to play no major role in the generation of subthreshold rhythmic membrane potential oscillations, because these persisted in the presence of Cs+. 6. On the other hand, in the SCs, the fast, sustained, outward rectification that strongly developed (after Na+ conductance block) at the oscillatory voltage level was not affected by Cs+ but was blocked by Ba2+ (1 mM). Barium was also effective in blocking the subthreshold membrane potential oscillations. 7. In the non-SCs, which do not generate subthreshold rhythmic membrane potential oscillations or manifest subthreshold outward rectification in TTX, Ca2+ conductance block abolished spike repolarization and caused the development of long-lasting Na(+)-dependent plateau potentials at a high suprathreshold voltage level. At this level, where prominent delayed rectification is present, the Na+ plateaus sustained rhythmic membrane potential oscillations.(ABSTRACT TRUNCATED AT 400 WORDS)

Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II

1993 ◽  
Vol 70 (1) ◽  
pp. 128-143 ◽  
Author(s):  
A. Alonso ◽  
R. Klink
Keyword(s):  
Membrane Potential ◽  
Entorhinal Cortex ◽  
Morphological Characteristics ◽  
Oscillatory Activity ◽  
Inward Rectification ◽  
Projection Neurons ◽  
Medial Entorhinal Cortex ◽  
Mean Frequency ◽  
Subthreshold Oscillations

1. The electroresponsive properties of neurons from layer II of the rat medial entorhinal cortex (MEC) were studied by intracellular recording under current clamp in an in vitro brain slice preparation. From a total of 184 cells that fulfilled our criteria for recording stability, two groups of projection neurons were distinguished on the basis of their intrinsic biophysical properties and morphological characteristics (demonstrated by intracellular biocytin injection; n = 34). 2. Stellate cells (SCs) were the most abundant (69%). They were highly electroresponsive, and minimal changes (1-3 mV) of membrane potential generated an active response. Subthreshold depolarizing or hyperpolarizing current pulse injection always caused the membrane potential to attain an early peak and then sag to a lower level. Depolarization-induced "sags" were larger and determined early firing in all cells. The voltage-current relationship of SCs was markedly non-linear, demonstrating robust inward rectification in the hyperpolarizing and depolarizing range. 3. SCs generated persistent rhythmic subthreshold voltage oscillations on DC depolarization positive to -60 mV. The mean frequency of the oscillations was 8.6 Hz (theta range) at a membrane potential of approximately -55 mV, at which level occasional single spiking also occurred. At slightly more positive potentials, a striking 1- to 3-Hz repetitive bursting pattern emerged. This consisted of nonadapting trains of spikes ("clusters") interspersed with subthreshold oscillations that had a mean frequency of 21.7 Hz (beta range). 4. Nonstellate cells (39%; mostly pyramidal-like) displayed time-dependent inward rectification that was less pronounced than that of SCs, and minimal depolarization-induced sags. On threshold depolarization, firing was always preceded by a slowly rising ramp depolarization and thus occurred with a long delay. Inward rectification in the depolarizing range was very pronounced. However, non-SCs did not generate persistent rhythmic subthreshold oscillatory activity or spike clusters. 5. Of the electrophysiological parameters quantified, spike threshold, spike duration, depolarizing afterpotential amplitude and apparent membrane time constant demonstrated statistically significant differences between SCs and non-SCs. 6. The repetitive hiring properties in response to square current pulses of short duration (< 500 ms) were also different between SCs and non-SCs. First, most SCs displayed a bilinear frequency-current (f-I) relationship for only the first interspike interval, whereas most non-SCs displayed a bilinear relationship for all intervals. Second, SCs had a much steeper primary f-I slope for early intervals than non-SCs. Finally, SCs displayed more pronounced and faster spike frequency adaptation than non-SCs.(ABSTRACT TRUNCATED AT 400 WORDS)

Subthreshold membrane potential oscillations in neurons of deep layers of the entorhinal cortex

Neuroscience ◽  
1998 ◽  
Vol 85 (4) ◽  
pp. 999-1004 ◽  
Author(s):  
D. Schmitz ◽  
T. Gloveli ◽  
J. Behr ◽  
T. Dugladze ◽  
U. Heinemann
Keyword(s):  
Membrane Potential ◽  
Entorhinal Cortex ◽  
Potential Oscillations ◽  
Deep Layers ◽  
Membrane Potential Oscillations

scholarly journals Autoactivity of A5 neurons: role of subthreshold oscillations and persistent Na+current

1997 ◽  
Vol 273 (5) ◽  
pp. H2280-H2289 ◽  
Author(s):  
Donghai Huangfu ◽  
Patrice G. Guyenet
Keyword(s):  
Membrane Potential ◽  
Discharge Rate ◽  
Input Resistance ◽  
Frequency Component ◽  
Inward Rectification ◽  
Intrinsic Properties ◽  
Potential Oscillations ◽  
Subthreshold Oscillations

A5 noradrenergic neurons play a key role in autonomic regulation, nociception, and respiration. The purpose of the present experiments was to characterize some of the intrinsic properties of A5 cells in vitro. Whole cell recordings were obtained from 85 spinally projecting neurons of the ventrolateral pons of neonate rats. Immunohistochemistry showed that 60% of the ventrolateral pontine cells were noradrenergic. Eighty percent of A5 neurons were spontaneously active (0.1–5.5 spikes/s). Their discharge rate was unchanged by a mixture of synaptic blockers that eliminated postsynaptic potentials (PSPs). The nonnoradrenergic cells could not be distinguished from A5 cells on the basis of discharge rate, action potential duration, inward rectification, input resistance, or accommodation. A5 cells displayed subthreshold irregular oscillations of the membrane potential (main frequency component 0.5–2 Hz). These oscillations were unchanged in the presence of low external Ca2+-high Mg2+ and were very reduced by hyperpolarizing the cells below −65 mV. The oscillations were partially attenuated by 1 μM tetrodotoxin (TTX) and were eliminated by reducing external Na+ (27 mM). Stepping the membrane potential from −65 to −50 mV for 200 ms revealed the presence of a transient and a persistent inward current that were both blocked by 0.1 μM TTX or by extracellular Na+ reduction. In conclusion, most A5 neurons are spontaneously active in vitro. They display irregular subthreshold membrane potential oscillations generated by voltage-activated conductances that include a persistent TTX-sensitive Na+ current. Most of the activity of A5 cells appears due to intrinsic properties rather than to synaptic inputs.

scholarly journals Linking Cellular Mechanisms to Behavior: Entorhinal Persistent Spiking and Membrane Potential Oscillations May Underlie Path Integration, Grid Cell Firing, and Episodic Memory

2008 ◽  
Vol 2008 ◽  
pp. 1-12 ◽  
Author(s):  
Michael E. Hasselmo ◽  
Mark P. Brandon
Keyword(s):  
Membrane Potential ◽  
Episodic Memory ◽  
Entorhinal Cortex ◽  
Path Integration ◽  
Grid Cell ◽  
Physiological Data ◽  
Cellular Mechanisms ◽  
Potential Oscillations ◽  
Cell Firing ◽  
Membrane Potential Oscillations

The entorhinal cortex plays an important role in spatial memory and episodic memory functions. These functions may result from cellular mechanisms for integration of the afferent input to entorhinal cortex. This article reviews physiological data on persistent spiking and membrane potential oscillations in entorhinal cortex then presents models showing how both these cellular mechanisms could contribute to properties observed during unit recording, including grid cell firing, and how they could underlie behavioural functions including path integration. The interaction of oscillations and persistent firing could contribute to encoding and retrieval of trajectories through space and time as a mechanism relevant to episodic memory.

scholarly journals 3-5 Hz membrane potential oscillations decrease the gain of neurons in visual cortex

2016 ◽  
Author(s):  
Michael C. Einstein ◽  
Pierre-Olivier Polack ◽  
Peyman Golshani
Keyword(s):  
Visual Cortex ◽  
Membrane Potential ◽  
Sensory Processing ◽  
Cortical Neurons ◽  
Visual Stimulation ◽  
Cellular Mechanisms ◽  
Potential Oscillations ◽  
Subthreshold Oscillations ◽  
Excitatory Neurons ◽  
Membrane Potential Oscillations

ABSTRACTGain modulation is a computational mechanism critical for sensory processing. Yet, the cellular mechanisms that decrease the gain of cortical neurons are unclear. To test if low frequency subthreshold oscillations could reduce neuronal gain during wakefulness, we measured the membrane potential of primary visual cortex (V1) layer 2/3 excitatory, parvalbumin-positive (PV+), and somatostatin-positive (SOM+) neurons in awake mice during passive visual stimulation and sensory discrimination tasks. We found prominent 3-5 Hz membrane potential oscillations that reduced the gain of excitatory neurons but not the gain of PV+ and SOM+ interneurons, which oscillated synchronously with excitatory neurons and fired strongly at the peak of de polarizations. 3-5 Hz oscillation prevalence and timing were strongly modulated by visual input and the animal’s behavior al response, suggesting that these oscillations are triggered to adjust sensory responses for specific behavioral contexts. Therefore, these findings reveal a novel gain reduction mechanism that adapts sensory processing to behavior.

­­Differential contribution of the subthreshold operating currents IT, Ih and IKir to the resonance of thalamocortical neurons

2021 ◽  
Author(s):  
Angela Isabel Tissone ◽  
Varinia Beatriz Vidal ◽  
Marcela Silvia Nadal ◽  
German Mato ◽  
Yimy Amarillo
Keyword(s):  
Membrane Potential ◽  
Brain Slices ◽  
Oscillatory Behavior ◽  
Negative Slope ◽  
Inward Rectification ◽  
Minor Role ◽  
Large Contribution ◽  
Potential Oscillations ◽  
Cationic Current ◽  
Membrane Potential Oscillations

Membrane potential oscillations of thalamocortical (TC) neurons are believed to be involved in the generation and maintenance of brain rhythms that underlie global physiological and pathological brain states. These membrane potential oscillations depend on the synaptic interactions of TC neurons and their intrinsic electrical properties. These oscillations may be also shaped by increased output responses at a preferred frequency, known as intrinsic neuronal resonance. Here we combine electrophysiological recordings in mouse brain slices, modern pharmacological tools, dynamic clamp and computational modeling to study the ionic mechanisms that generate and modulate TC neuron resonance. We confirm findings of pioneering studies showing that most TC neurons display resonance which results from the interaction of the slow inactivation of the low threshold calcium current IT with the passive properties of the membrane. We also show that the hyperpolarization activated cationic current Ih is not involved in the generation of resonance, instead, it plays a minor role in the stabilization of TC neuron impedance magnitude due to its large contribution to the steady conductance. More importantly, we also demonstrate that TC neuron resonance is amplified by the inward rectifier potassium current IKir by a mechanism that hinges on its strong voltage dependent inward rectification (i.e. a negative slope conductance region) Accumulating evidence indicate that the ion channels that control the oscillatory behavior of TC neurons participate in pathophysiological processes. Results presented here points to IKir as a new potential target for therapeutic intervention.

Cell-Type–Specific Modulation of Intrinsic Firing Properties and Subthreshold Membrane Oscillations by the M(Kv7)-Current in Neurons of the Entorhinal Cortex

2007 ◽  
Vol 98 (5) ◽  
pp. 2779-2794 ◽  
Author(s):  
Motoharu Yoshida ◽  
Angel Alonso
Keyword(s):  
Membrane Potential ◽  
Entorhinal Cortex ◽  
Intrinsic Excitability ◽  
Cell Type ◽  
Potential Oscillations ◽  
Principal Cells ◽  
M Current ◽  
Current Block ◽  
Layer V ◽  
Membrane Potential Oscillations

The M-current (current through Kv7 channels) is a low-threshold noninactivating potassium current that is suppressed by muscarinic agonists. Recent studies have shown its role in spike burst generation and intrinsic subthreshold theta resonance, both of which are important for memory function. However, little is known about its role in principal cells of the entorhinal cortex (EC). In this study, using whole cell patch recording techniques in a rat EC slice preparation, we have examined the effects of the M-current blockers linopirdine and XE991 on the membrane dynamics of principal cells in the EC. When the M-current was blocked, layer II nonstellate cells (non-SCs) and layer III cells switched from tonic discharge to intermittent firing mode, during which layer II non-SCs showed high-frequency short-duration spike bursts due to increased fast spike afterdepolarization (ADP). When three spikes were elicited at 50 Hz, these two types of cells reacted with a slow ADP that drove delayed firing. In contrast, layer II stellate cells (SCs) and layer V cells never displayed intermittent firing, bursting behavior, or delayed firing. Under the M-current block, intrinsic excitability increased significantly in layer III and layer V cells but not in layer II SCs and non-SCs. The M-current block also had contrasting effects on the subthreshold excitability, greatly suppressing the subthreshold membrane potential oscillations in layer V cells but not in layer II SCs. Modulation of the M-current thus shifts the firing behavior, intrinsic excitability, and subthreshold membrane potential oscillations of EC principal cells in a cell-type–dependent manner.

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