scholarly journals Serotonin excites hippocampal CA1 GABAergic interneurons at the stratum radiatum-stratum lacunosum moleculare border

Hippocampus ◽  
2016 ◽  
Vol 26 (9) ◽  
pp. 1107-1114 ◽  
Author(s):  
Daniel R. Wyskiel ◽  
Rodrigo Andrade
Keyword(s):  
Stratum Radiatum ◽  
Gabaergic Interneurons ◽  
Hippocampal Ca1 ◽  
Stratum Lacunosum Moleculare

Intrinsic Theta-Frequency Membrane Potential Oscillations in Hippocampal CA1 Interneurons of Stratum Lacunosum-Moleculare

1999 ◽  
Vol 81 (3) ◽  
pp. 1296-1307 ◽  
Author(s):  
C. Andrew Chapman ◽  
Jean-Claude Lacaille
Keyword(s):  
Membrane Potential ◽  
Hippocampal Slices ◽  
Stratum Radiatum ◽  
Potential Oscillations ◽  
Spike Threshold ◽  
Hippocampal Ca1 ◽  
Theta Frequency ◽  
Stratum Lacunosum Moleculare ◽  
Membrane Potential Oscillations

Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. The ionic conductances underlying membrane potential oscillations of hippocampal CA1 interneurons located near the border between stratum lacunosum-moleculare and stratum radiatum (LM) were investigated using whole cell current-clamp recordings in rat hippocampal slices. At 22°C, when LM cells were depolarized near spike threshold by current injection, 91% of cells displayed 2–5 Hz oscillations in membrane potential, which caused rhythmic firing. At 32°C, mean oscillation frequency increased to 7.1 Hz. Oscillations were voltage dependent and were eliminated by hyperpolarizing cells 6–10 mV below spike threshold. Blockade of ionotropic glutamate and GABA synaptic transmission did not affect oscillations, indicating that they were not synaptically driven. Oscillations were eliminated by tetrodotoxin, suggesting that Na+ currents generate the depolarizing phase of oscillations. Oscillations were not affected by blocking Ca2+ currents with Cd2+ or Ca2+-free ACSF or by blocking the hyperpolarization-activated current ( I h) with Cs+. Both Ba2+ and a low concentration of 4-aminopyridine (4-AP) reduced oscillations but TEA did not. Theta-frequency oscillations were much less common in interneurons located in stratum oriens. Intrinsic membrane potential oscillations in LM cells of the CA1 region thus involve an interplay between inward Na+ currents and outward K+ currents sensitive to Ba2+ and 4-AP. These oscillations may participate in rhythmic inhibition and synchronization of pyramidal neurons during theta activity in vivo.

Cell-Specific Alterations in Synaptic Properties of Hippocampal CA1 Interneurons After Kainate Treatment

1998 ◽  
Vol 80 (6) ◽  
pp. 2836-2847 ◽  
Author(s):  
F. Morin ◽  
C. Beaulieu ◽  
J.-C. Lacaille
Keyword(s):  
Time Constant ◽  
Decay Time ◽  
Pyramidal Cells ◽  
Stratum Radiatum ◽  
Inhibitory Interneurons ◽  
Cell Type ◽  
Postsynaptic Currents ◽  
Ca1 Region ◽  
Hippocampal Ca1 ◽  
Stratum Lacunosum Moleculare

Morin, F., C. Beaulieu, and J.-C. Lacaille. Cell-specific alterations in synaptic properties of hippocampal CA1 interneurons after kainate treatment. J. Neurophysiol. 80: 2836–2847, 1998. Hippocampal sclerosis and hyperexcitability are neuropathological features of human temporal lobe epilepsy that are reproduced in the kainic acid (KA) model of epilepsy in rats. To assess directly the role of inhibitory interneurons in the KA model, the membrane and synaptic properties of interneurons located in 1) stratum oriens near the alveus (O/A) and 2) at the border of stratum radiatum and stratum lacunosum-moleculare (LM), as well as those of pyramidal cells, were examined with whole cell recordings in slices of control and KA-lesioned rats. In current-clamp recordings, intrinsic cell properties such as action potential amplitude and duration, amplitude of fast and medium duration afterhyperpolarizations, membrane time constant, and input resistance were generally unchanged in all cell types after KA treatment. In voltage-clamp recordings, the amplitude and conductance of pharmacologically isolated excitatory postsynaptic currents (EPSCs) were significantly reduced in LM interneurons of KA-treated animals but were not significantly changed in O/A and pyramidal cells. The rise time of EPSCs was not significantly changed in any cell type after KA treatment. In contrast, the decay time constant of EPSCs was significantly faster in O/A interneurons of KA-treated rats but was unchanged in LM and pyramidal cells. The amplitude and conductance of pharmacologically isolated γ-aminobutyric acid-A (GABAA) inhibitory postsynaptic currents (IPSCs) were not significantly changed in any cell type of KA-treated rats. The rise time and decay time constant of GABAA IPSCs were significantly faster in pyramidal cells of KA-treated rats but were not significantly changed in O/A and LM interneurons. These results suggest that complex alterations in synaptic currents occur in specific subpopulations of inhibitory interneurons in the CA1 region after KA lesions. A reduction of evoked excitatory drive onto inhibitory cells located at the border of stratum radiatum and stratum lacunosum-moleculare may contribute to disinhibition and polysynaptic epileptiform activity in the CA1 region. Compensatory changes, involving excitatory synaptic transmission on other interneuron subtypes and inhibitory synaptic transmission on pyramidal cells, may also take place and contribute to the residual, functional monosynaptic inhibition observed in principal cells after KA treatment.

IPSPs modulate spike backpropagation and associated [Ca2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons

1996 ◽  
Vol 76 (5) ◽  
pp. 2896-2906 ◽  
Author(s):  
H. Tsubokawa ◽  
W. N. Ross
Keyword(s):  
Action Potentials ◽  
Pyramidal Neurons ◽  
Time Window ◽  
Proximal Part ◽  
Stratum Radiatum ◽  
Ca1 Pyramidal Neurons ◽  
Hippocampal Ca1 ◽  
Dendritic Branches ◽  
Apical Dendrites ◽  
Stratum Lacunosum Moleculare

1. We studied the effects of synaptic inhibition on backpropagating Na+ spikes in the apical dendrites of CA1 pyramidal neurons in transverse slices from the rat hippocampus. Action potentials were evoked synaptically by stimulation in the stratum radiatum or antidromically by stimulation in the alveus. 2. Inhibitory postsynaptic potentials, evoked by stimulation in the stratum lacunosum moleculare, reduced the amplitude of single spikes in the distal dendrites but did not change the amplitudes in the somatic or proximal regions. Inhibition also reduced the spike-associated [Ca2+]i changes in the distal dendrites but had little effect on the changes in the proximal part of the cell. Both of these results are consistent with inhibition converting actively backpropagating spikes into passively spreading potentials at some point in the arbor. 3. In most cells, the spike amplitude reduction in the distal dendrites was blocked by bicuculline methiodide (10 microM) and inhibition was most effective when evoked in a time window < 10 ms preceding the action potential. This suggests that the amplitude reduction was due to a conductance shunt activated by gamma-aminobuturic acid-A (GABAA) receptors. Synaptically evoked GABAB responses were detected but usually did not block spike propagation. 4. Direct hyperpolarization in the distal dendrites was also effective in blocking antidromically evoked spike backpropagation but probably does not contribute when the action potentials are evoked synaptically. 5. This effect of inhibition is different from its usual function in synaptic integration because spike generation and propagation down the axon are not significantly affected. This kind of inhibition might be important in regulating transient [Ca2+]i changes in the dendrites including individual dendritic branches.

Ultrastructure of stratum lacunosum moleculare interneurons of hippocampal CA1 region

Synapse ◽  
1988 ◽  
Vol 2 (4) ◽  
pp. 382-394 ◽  
Author(s):  
Dennis D. Kunkel ◽  
Jean-Claude Lacaille ◽  
Philip A. Schwartzkroin
Keyword(s):  
Ca1 Region ◽  
Hippocampal Ca1 Region ◽  
Hippocampal Ca1 ◽  
Stratum Lacunosum Moleculare

Ca2+ Ions Block and Permeate Serotonin 5-HT3 Receptor Channels in Rat Hippocampal Interneurons

2003 ◽  
Vol 89 (4) ◽  
pp. 1864-1869 ◽  
Author(s):  
Johannes A. van Hooft ◽  
Wytse J. Wadman
Keyword(s):  
Binding Sites ◽  
Membrane Potentials ◽  
Ion Current ◽  
Stratum Radiatum ◽  
Negative Slope ◽  
Rate Theory ◽  
Dependent Manner ◽  
Site Model ◽  
Hippocampal Ca1 ◽  
Voltage Dependent

The serotonin 5-HT3receptor native to rat hippocampal CA1 stratum radiatum interneurons is blocked by Ca2+ ions in a dose- and voltage-dependent manner, which is reflected by a region of negative slope conductance in the I-V curve. The steep dependence on the extracellular Ca2+concentration suggests that the channel contains more than one binding site for Ca2+. A three barrier-two site model, based on Eyring rate theory, was used to describe the I-Vcurves. When extra- and intracellular K+ and Cs+ were substituted with Na+, the I-V curves were accurately fit by the model, unlike the I-V curves recorded under standard ionic conditions. This suggests that the K+ and Cs+ permeabilities are small compared with that of Na+. The distribution of the energy barriers and binding sites for Ca2+ and Na+ showed that the binding sites are located at approximately the 13′ and the –4′ position in the ion channel. The model predicts that at large hyperpolarized membrane potentials (more negative than −120 mV), the fractional Ca2+ current amounts to approximately 1% of the total ion current. However, at physiologically relevant membrane potentials, the fractional Ca2+ current is smaller (<0.1%) and the relative Ca2+permeability ( P Ca/ P Na) is estimated to be 0.10 at –60 mV.

Inhibitory processes of hippocampal CA1 pyramidal neurons following kindling-induced epilepsy in the rat

1985 ◽  
Vol 63 (7) ◽  
pp. 872-878 ◽  
Author(s):  
M. W. Oliver ◽  
J. J. Miller
Keyword(s):  
Pyramidal Neurons ◽  
Epileptiform Activity ◽  
Pyramidal Cells ◽  
Repetitive Stimulation ◽  
Membrane Properties ◽  
Stratum Radiatum ◽  
Inhibitory Processes ◽  
Ca1 Pyramidal Neurons ◽  
Hippocampal Ca1 ◽  
Stimulation Of

To determine the alterations in cellular function which may contribute to the chronic predisposition of neuronal tissue to epileptiform activity, the membrane properties and inhibitory processes of hippocampal CA1 pyramidal cells were investigated using in vitro slices prepared from commissural-kindled rats. No changes were observed in resting membrane potential, input resistance, spike amplitude, and membrane time constant of "kindled" CA1 pyramidal neurons when compared with controls. There were also no differences between control and kindled preparations in the amplitude of recurrent inhibitory postsynaptic potentials (IPSP) and in the duration of inhibition produced by either alvear (Alv) or stratum radiatum (SR) stimulation. Irrespective of group, repetitive stimulation of the Alv reduced the amplitude of the recurrent IPSP but failed to induce seizurelike activity. On the other hand, repetitive stimulation of SR frequently produced a neuronal burst discharge even though the duration and to some extent the amplitude of orthodromic inhibition was increased. On the basis of these data, it may be suggested that chronic changes in CA1 pyramidal cell membrane properties and transient reductions of inhibitory processes do not underlie the enhanced sensitivity of these neurons to seizure activity associated with kindling.

scholarly journals Acetylcholine release inhibits distinct excitatory inputs onto hippocampal CA1 pyramidal neurons via different cellular and network mechanisms

2019 ◽  
Author(s):  
Priyodarshan Goswamee ◽  
A. Rory McQuiston
Keyword(s):  
Receptor Antagonist ◽  
Brain Slices ◽  
Pyramidal Cells ◽  
Inhibitory Interneuron ◽  
Stratum Radiatum ◽  
Synaptic Efficacy ◽  
Ach Release ◽  
Paired Pulse ◽  
Ca1 Pyramidal Cells ◽  
Hippocampal Ca1

AbstractIn hippocampal CA1, muscarinic acetylcholine (ACh) receptor (mAChR) activation via exogenous application of cholinergic agonists has been shown to presynaptically inhibit Schaffer collateral (SC) glutamatergic inputs in stratum radiatum (SR), and temporoammonic (TA) and thalamic nucleus reuniens (RE) glutamatergic inputs in stratum lacunosum-moleculare (SLM). However, steady-state uniform mAChR activation may not mimic the effect of ACh release in an intact hippocampal network. To more accurately examine the effect of ACh release on glutamatergic synaptic efficacy, we measured electrically evoked synaptic responses in CA1 pyramidal cells (PCs) following the optogenetic release of ACh in genetically modified mouse brain slices. The ratio of synaptic amplitudes in response to paired-pulse SR stimulation (stimulus 2/stimulus 1) was significantly reduced by the optogenetic release of ACh, consistent with a postsynaptic decrease in synaptic efficacy. The effect of ACh release was blocked by the M3 receptor antagonist 4-DAMP, the GABAB receptor antagonist CGP 52432, inclusion of GDP-β-S, cesium, QX314 in the intracellular patch clamp solution, or extracellular barium. These observations suggest that ACh release decreased SC synaptic transmission through an M3 muscarinic receptor-mediated increase in inhibitory interneuron excitability, which activate GABAB receptors and inwardly rectifying potassium channels on CA1 pyramidal cells. In contrast, the ratio of synaptic amplitudes in response to paired-pulse stimulation in the SLM was increased by ACh release, consistent with presynaptic inhibition. ACh-mediated effects in SLM were blocked by the M2 receptor antagonist AF-DX 116, presumably located on presynaptic terminals. Therefore, our data indicate that ACh release differentially modulates excitatory inputs in SR and SLM of CA1 through different cellular and network mechanisms.

Comparable GABAergic Mechanisms of Hippocampal Seizurelike Activity in Posttetanic and Low-Mg2+ Conditions

2006 ◽  
Vol 95 (3) ◽  
pp. 2013-2019 ◽  
Author(s):  
Yoko Fujiwara-Tsukamoto ◽  
Yoshikazu Isomura ◽  
Masahiko Takada
Keyword(s):  
Seizure Activity ◽  
Extracellular Fluid ◽  
Pyramidal Cells ◽  
Gabaergic Interneurons ◽  
Tetanic Stimulation ◽  
Inhibitory Neurotransmitter ◽  
Ca1 Pyramidal Cells ◽  
Ca1 Region ◽  
Hippocampal Ca1 ◽  
Oscillatory Response

It is known that GABA is a major inhibitory neurotransmitter in mature mammalian brains, but the effect of this substance is sometimes converted into depolarizing or even excitatory when the postsynaptic Cl– concentration becomes high. Recently we have shown that seizurelike afterdischarge induced by tetanic stimulation in normal extracellular fluid (posttetanic afterdischarge) is mediated through GABAergic excitation in mature hippocampal CA1 pyramidal cells. In this study, we examined the possible contribution of similar depolarizing/excitatory GABAergic input to the CA1 pyramidal cells to the seizurelike afterdischarge induced in a low extracellular Mg2+ condition, another experimental model of epileptic seizure activity (low-Mg2+ afterdischarge). Perfusion of the GABAA antagonist bicuculline abolished the low-Mg2+ afterdischarge, but not the interictal-like activity, in most cases. Each oscillatory response during the low-Mg2+ afterdischarge was dependent on Cl– conductance and contained an F–-insensitive depolarizing component in the pyramidal cells, thus indicating that the afterdischarge response may be mediated through both GABAergic and nonGABAergic transmissions. In addition, local GABA application to the recorded cells revealed that GABA responses were indeed depolarizing during the low-Mg2+ afterdischarge. Furthermore, the GABAergic interneurons located in the strata pyramidale and oriens fired in oscillatory cycles more actively than those in other layers of the CA1 region. These results suggest that the depolarizing GABAergic input may facilitate oscillatory synchronization among the hippocampal CA1 pyramidal cells during the low-Mg2+ afterdischarge in a manner similar to the expression of the posttetanic afterdischarge.

Sign in / Sign up

Export Citation Format

Share Document