Frequency of Subthreshold Oscillations at Different Membrane Potential Voltages in Neurons at Different Anatomical Positions on the Dorsoventral Axis in the Rat Medial Entorhinal Cortex

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)

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

Journal of Neurophysiology ◽

10.1152/jn.1993.70.1.128 ◽

1993 ◽

Vol 70 (1) ◽

pp. 128-143 ◽

Cited By ~ 279

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)

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Frequency Selectivity of Layer II Stellate Cells in the Medial Entorhinal Cortex

Journal of Neurophysiology ◽

10.1152/jn.00598.2002 ◽

2002 ◽

Vol 88 (5) ◽

pp. 2422-2429 ◽

Cited By ~ 95

Author(s):

Julie S. Haas ◽

John A. White

Keyword(s):

Entorhinal Cortex ◽

Stellate Cells ◽

Mechanistic Explanation ◽

Input Power ◽

Total Power ◽

Frequency Content ◽

Medial Entorhinal Cortex ◽

Subthreshold Oscillations ◽

Subthreshold Resonance

Electrophysiologically, stellate cells (SCs) from layer II of the medial entorhinal cortex (MEC) are distinguished by intrinsic 4- to 12-Hz subthreshold oscillations. These oscillations are thought to impose a pattern of slow periodic firing that may contribute to the parahippocampal theta rhythm in vivo. Using stimuli with systematically differing frequency content, we examined supra- and subthreshold responses in SCs with the goal of understanding how their distinctive characteristics shape these responses. In reaction to repeated presentations of identical, pseudo-random stimuli, the reliability (repeatability) of the spiking response in SCs depends critically on the frequency content of the stimulus. Reliability is optimal for stimuli with a greater proportion of power in the 4- to 12-Hz range. The simplest mechanistic explanation of these results is that rhythmogenic subthreshold membrane mechanisms resonate with inputs containing significant power in the 4- to 12-Hz band, leading to larger subthreshold excursions and thus enhanced reliability. However, close examination of responses rules out this explanation: SCs do show clear subthreshold resonance (i.e., selective amplification of inputs with particular frequency content) in response to sinusoidal stimuli, while simultaneously showing a lack of subthreshold resonance in response to the pseudo-random stimuli used in reliability experiments. Our results support a model with distinctive input-output relationships under subthreshold and suprathreshold conditions. For suprathreshold stimuli, SC spiking seems to best reflect the amount of input power in the theta (4–12 Hz) frequency band. For subthreshold stimuli, we hypothesize that the magnitude of subthreshold theta-range oscillations in SCs reflects the total power, across all frequencies, of the input.

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Inhibitory Gradient along the Dorsoventral Axis in the Medial Entorhinal Cortex

Neuron ◽

10.1016/j.neuron.2013.06.038 ◽

2013 ◽

Vol 79 (6) ◽

pp. 1197-1207 ◽

Cited By ~ 54

Author(s):

Prateep Beed ◽

Anja Gundlfinger ◽

Sophie Schneiderbauer ◽

Jie Song ◽

Claudia Böhm ◽

...

Keyword(s):

Entorhinal Cortex ◽

Medial Entorhinal Cortex ◽

Dorsoventral Axis

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Subthreshold Membrane-Potential Resonances Shape Spike-Train Patterns in the Entorhinal Cortex

Journal of Neurophysiology ◽

10.1152/jn.01282.2007 ◽

2008 ◽

Vol 100 (3) ◽

pp. 1576-1589 ◽

Cited By ~ 72

Author(s):

T. A. Engel ◽

L. Schimansky-Geier ◽

A.V.M. Herz ◽

S. Schreiber ◽

I. Erchova

Keyword(s):

Membrane Potential ◽

Entorhinal Cortex ◽

Rhythmic Activity ◽

Cell Types ◽

Neuronal Firing ◽

Type Model ◽

Fundamental Properties ◽

Subthreshold Oscillations ◽

Subthreshold Resonance ◽

Specific Discharge

Many neurons exhibit subthreshold membrane-potential resonances, such that the largest voltage responses occur at preferred stimulation frequencies. Because subthreshold resonances are known to influence the rhythmic activity at the network level, it is vital to understand how they affect spike generation on the single-cell level. We therefore investigated both resonant and nonresonant neurons of rat entorhinal cortex. A minimal resonate-and-fire type model based on measured physiological parameters captures fundamental properties of neuronal firing statistics surprisingly well and helps to shed light on the mechanisms that shape spike patterns: 1) subthreshold resonance together with a spike-induced reset of subthreshold oscillations leads to spike clustering and 2) spike-induced dynamics influence the fine structure of interspike interval (ISI) distributions and are responsible for ISI correlations appearing at higher firing rates (≥3 Hz). Both mechanisms are likely to account for the specific discharge characteristics of various cell types.

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Parvalbumin Interneurons Are Differentially Connected to Principal Cells in Inhibitory Feedback Microcircuits along the Dorsoventral Axis of the Medial Entorhinal Cortex

eNeuro ◽

10.1523/eneuro.0354-20.2020 ◽

2021 ◽

Vol 8 (1) ◽

pp. ENEURO.0354-20.2020

Author(s):

Sabine Grosser ◽

Federico J. Barreda ◽

Prateep Beed ◽

Dietmar Schmitz ◽

Sam A. Booker ◽

...

Keyword(s):

Entorhinal Cortex ◽

Medial Entorhinal Cortex ◽

Dorsoventral Axis ◽

Principal Cells ◽

Parvalbumin Interneurons ◽

Inhibitory Feedback

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Mouse entorhinal cortex encodes a diverse repertoire of self-motion signals

Nature Communications ◽

10.1038/s41467-021-20936-8 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Caitlin S. Mallory ◽

Kiah Hardcastle ◽

Malcolm G. Campbell ◽

Alexander Attinger ◽

Isabel I. C. Low ◽

...

Keyword(s):

Entorhinal Cortex ◽

Medial Temporal Lobe ◽

Visual Cues ◽

Neural Circuits ◽

Sensory Cues ◽

Medial Entorhinal Cortex ◽

Representation Of Space ◽

Self Motion ◽

Information Streams ◽

Representations Of Space

AbstractNeural circuits generate representations of the external world from multiple information streams. The navigation system provides an exceptional lens through which we may gain insights about how such computations are implemented. Neural circuits in the medial temporal lobe construct a map-like representation of space that supports navigation. This computation integrates multiple sensory cues, and, in addition, is thought to require cues related to the individual’s movement through the environment. Here, we identify multiple self-motion signals, related to the position and velocity of the head and eyes, encoded by neurons in a key node of the navigation circuitry of mice, the medial entorhinal cortex (MEC). The representation of these signals is highly integrated with other cues in individual neurons. Such information could be used to compute the allocentric location of landmarks from visual cues and to generate internal representations of space.

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