scholarly journals Fast-spiking Cell to Pyramidal Cell Connections Are the Most Sensitive to Propofol-induced Facilitation of GABAergic Currents in Rat Insular Cortex

2014 ◽  
Vol 121 (1) ◽  
pp. 68-78 ◽  
Author(s):  
Yuko Koyanagi ◽  
Yoshiyuki Oi ◽  
Kiyofumi Yamamoto ◽  
Noriaki Koshikawa ◽  
Masayuki Kobayashi
Keyword(s):  
Charge Transfer ◽  
Synaptic Transmission ◽  
Insular Cortex ◽  
Pyramidal Cells ◽  
Projection Neurons ◽  
Decay Kinetics ◽  
Patch Clamp Recording ◽  
Whole Cell Patch Clamp ◽  
Fast Spiking ◽  
Local Circuits

Abstract Background: Propofol facilitates γ-aminobutyric acid–mediated inhibitory synaptic transmission. In the cerebral cortex, γ-aminobutyric acidergic interneurons target both excitatory pyramidal cells (Pyr) and fast-spiking (FS) and non-FS interneurons. Therefore, the propofol-induced facilitation of inhibitory transmission results in a change in the balance of excitatory and inhibitory inputs to Pyr. However, it is still unknown how propofol modulates γ-aminobutyric acidergic synaptic transmission in each combination of Pyr and interneurons. Methods: The authors examined whether propofol differentially regulates inhibitory postsynaptic currents (IPSCs) depending on the presynaptic and postsynaptic cell subtypes using multiple whole cell patch clamp recording from γ-aminobutyric acidergic interneurons and Pyr in rat insular cortex. Results: Propofol (10 μM) consistently prolonged decay kinetics of unitary IPSCs (uIPSCs) in all types of inhibitory connections without changing paired-pulse ratio of the second to first uIPSC amplitude or failure rate. The FS→Pyr connections exhibited greater enhancement of uIPSC charge transfer (2.2 ± 0.5 pC, n = 36) compared with that of FS→FS/non-FS connections (0.9 ± 0.2 pC, n = 37), whereas the enhancement of charge transfer in non-FS→Pyr (0.3 ± 0.1 pC, n = 15) and non-FS→FS/non-FS connections (0.2 ± 0.1 pC, n = 36) was smaller to those in FS→Pyr/FS/non-FS. Electrical synapses between FS pairs were not affected by propofol. Conclusions: The principal inhibitory connections (FS→Pyr) are the most sensitive to propofol-induced facilitation of uIPSCs, which is likely mediated by postsynaptic mechanisms. This preferential uIPSC enhancement in FS→Pyr connections may result in suppressed neural activities of projection neurons, which in turn reduces excitatory outputs from cortical local circuits.

Postsynaptic Cell Type–Dependent Cholinergic Regulation of GABAergic Synaptic Transmission in Rat Insular Cortex

2010 ◽  
Vol 104 (4) ◽  
pp. 1933-1945 ◽  
Author(s):  
Kiyofumi Yamamoto ◽  
Yuko Koyanagi ◽  
Noriaki Koshikawa ◽  
Masayuki Kobayashi
Keyword(s):  
Synaptic Transmission ◽  
Pyramidal Cell ◽  
Insular Cortex ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Patch Clamp Recording ◽  
Electrophysiological Properties ◽  
Heterogeneous Effects ◽  
Postsynaptic Cell ◽  
Gabaergic Synaptic Transmission

The cerebral cortex consists of multiple neuron subtypes whose electrophysiological properties exhibit diverse modulation patterns in response to neurotransmitters, including noradrenaline and acetylcholine (ACh). We performed multiple whole cell patch-clamp recording from layer V GABAergic interneurons and pyramidal cells of rat insular cortex (IC) to examine whether cholinergic effects on unitary inhibitory postsynaptic currents (uIPSCs) are differentially regulated by ACh receptors, depending on their presynaptic and postsynaptic cell subtypes. In fast-spiking (FS) to pyramidal cell synapses, carbachol (10 μM) invariably decreased uIPSC amplitude by 51.0%, accompanied by increases in paired-pulse ratio (PPR) of the second to first uIPSC amplitude, coefficient of variation (CV) of the first uIPSC amplitude, and failure rate. Carbachol-induced uIPSC suppression was dose dependent and blocked by atropine, a muscarinic ACh receptor antagonist. Similar cholinergic suppression was observed in non-FS to pyramidal cell synapses. In contrast, FS to FS/non-FS cell synapses showed heterogeneous effects on uIPSC amplitude by carbachol. In roughly 40% of pairs, carbachol suppressed uIPSCs by 35.8%, whereas in a similar percentage of pairs uIPSCs were increased by 34.8%. Non-FS to FS/non-FS cell synapses also showed carbachol-induced uIPSC facilitation by 29.2% in about half of the pairs, whereas nearly 40% of pairs showed carbachol-induced suppression of uIPSCs by 40.3%. Carbachol tended to increase uIPSC amplitude in interneuron-to-interneuron synapses with higher PPR, suggesting that carbachol facilitates GABA release in interneuron synapses with lower release probability. These results suggest that carbachol-induced effects on uIPSCs are not homogeneous but preiotropic: i.e., cholinergic modulation of GABAergic synaptic transmission is differentially regulated depending on postsynaptic neuron subtypes.

Kinetics of GABAB autoreceptor-mediated suppression of GABA release in rat insular cortex

2012 ◽  
Vol 107 (5) ◽  
pp. 1431-1442 ◽  
Author(s):  
Masayuki Kobayashi ◽  
Hiroki Takei ◽  
Kiyofumi Yamamoto ◽  
Hiroshige Hatanaka ◽  
Noriaki Koshikawa
Keyword(s):  
Insular Cortex ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Paired Pulse ◽  
Whole Cell Patch Clamp ◽  
Pulse Ratio ◽  
Presynaptic Mechanisms ◽  
Fast Spiking ◽  
Layer V ◽  
Interevent Interval

Release of GABA is controlled by presynaptic GABA receptor type B (GABAB) autoreceptors at GABAergic terminals. However, there is no direct evidence that GABAB autoreceptors are activated by GABA release from their own terminals, and precise profiles of GABAB autoreceptor-mediated suppression of GABA release remain unknown. To explore these issues, we performed multiple whole-cell, patch-clamp recordings from layer V rat insular cortex. Both unitary inhibitory and excitatory postsynaptic currents (uIPSCs and uEPSCs, respectively) were recorded by applying a five-train depolarizing pulse injection at 20 Hz. In connections from both fast-spiking (FS) and non-FS interneurons to pyramidal cells, the GABAB receptor antagonist CGP 52432 had little effect on the initial uIPSC amplitude. However, uIPSCs, responding to later pulses, were effectively facilitated. This CGP 52432-induced facilitation was prominent in the fourth uIPSCs, which were evoked 150 ms after the first uIPSC. The facilitation of uIPSCs was accompanied by an increase in the paired-pulse ratio. In addition, analysis of the coefficient of variation suggests the involvement of presynaptic mechanisms in CGP 52432-induced uIPSC facilitation. Paired-pulse stimulation (interstimulus interval = 150 ms) of presynaptic FS cells revealed that the second uIPSC was also facilitated by CGP 52432, which had little effect on the amplitude and interevent interval of miniature IPSCs. In contrast, uEPSCs, responding to all five stimulations of a presynaptic pyramidal cell, were less affected by CGP 52432. These results suggest that a single presynaptic action potential is sufficient to activate GABAB autoreceptors and to suppress GABA release in the cerebral cortex.

Presynaptic Interneuron Subtype- and Age-Dependent Modulation of GABAergic Synaptic Transmission by β-Adrenoceptors in Rat Insular Cortex

2010 ◽  
Vol 103 (5) ◽  
pp. 2876-2888 ◽  
Author(s):  
Yuko Koyanagi ◽  
Kiyofumi Yamamoto ◽  
Yoshiyuki Oi ◽  
Noriaki Koshikawa ◽  
Masayuki Kobayashi
Keyword(s):  
Synaptic Transmission ◽  
Pyramidal Cell ◽  
Insular Cortex ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Taste Aversion Learning ◽  
Inhibitory Synaptic Transmission ◽  
Whole Cell Patch Clamp ◽  
Adrenergic Modulation ◽  
Layer V

β-Adrenoceptors play a crucial role in the regulation of taste aversion learning in the insular cortex (IC). However, β-adrenergic effects on inhibitory synaptic transmission mediated by γ-aminobutyric acid (GABA) remain unknown. To elucidate the mechanisms of β-adrenergic modulation of inhibitory synaptic transmission, we performed paired whole cell patch-clamp recordings from layer V GABAergic interneurons and pyramidal cells of rat IC aged from postnatal day 17 (PD17) to PD46 and examined the effects of isoproterenol, a β-adrenoceptor agonist, on unitary inhibitory postsynaptic currents (uIPSCs). Isoproterenol (100 μM) induced facilitating effects on uIPSCs in 33.3% of cell pairs accompanied by decreases in coefficient of variation (CV) of the first uIPSC amplitude and paired-pulse ratio (PPR) of the second to first uIPSC amplitude, whereas 35.9% of pairs showed suppressive effects of isoproterenol on uIPSC amplitude obtained from fast spiking (FS) to pyramidal cell pairs. Facilitatory effects of isoproterenol were frequently observed in FS–pyramidal cell pairs at ≥PD24. On the other hand, isoproterenol suppressed uIPSC amplitude by 52.3 and 39.8% in low-threshold spike (LTS)–pyramidal and late spiking (LS)–pyramidal cell pairs, respectively, with increases in CV and PPR. The isoproterenol-induced suppressive effects were blocked by preapplication of 100 μM propranolol, a β-adrenoceptor antagonist. There was no significant correlation between age and changes of uIPSCs in LTS–/LS–pyramidal cell pairs. These results suggest the presence of differential mechanisms in presynaptic GABA release and/or postsynaptic GABAA receptor-related assemblies among interneuron subtypes. Age- and interneuron subtype-specific β-adrenergic modulation of IPSCs may contribute to experience-dependent plasticity in the IC.

Kainate receptor-mediated synaptic transmissions in the adult rodent insular cortex

2012 ◽  
Vol 108 (7) ◽  
pp. 1988-1998 ◽  
Author(s):  
Kohei Koga ◽  
Su-Eon Sim ◽  
Tao Chen ◽  
Long-Jun Wu ◽  
Bong-Kiun Kaang ◽  
...  
Keyword(s):  
Synaptic Transmission ◽  
Receptor Antagonist ◽  
Ampa Receptor ◽  
Time Course ◽  
Insular Cortex ◽  
Nmda Receptor Antagonist ◽  
Functional Roles ◽  
Adult Rat ◽  
Whole Cell Patch Clamp ◽  
The Central Nervous System

Kainate (KA) receptors are expressed widely in the central nervous system and regulate both excitatory and inhibitory synaptic transmission. KA receptors play important roles in fear memory, anxiety, and pain. However, little is known about their function in synaptic transmission in the insular cortex (IC), a critical region for taste, memory, and pain. Using whole cell patch-clamp recordings, we have shown that KA receptors contribute to fast synaptic transmission in neurons in all layers of the IC. In the presence of the GABAA receptor antagonist picrotoxin, the NMDA receptor antagonist AP-5, and the selective AMPA receptor antagonist GYKI 53655, KA receptor-mediated excitatory postsynaptic currents (KA EPSCs) were revealed. We found that KA EPSCs are ∼5–10% of AMPA/KA EPSCs in all layers of the adult mouse IC. Similar results were found in adult rat IC. KA EPSCs had a significantly slower rise time course and decay time constant compared with AMPA receptor-mediated EPSCs. High-frequency repetitive stimulations at 200 Hz significantly facilitated the summation of KA EPSCs. In addition, genetic deletion of GluK1 or GluK2 subunit partially reduced postsynaptic KA EPSCs, and exposure of GluK2 knockout mice to the selective GluK1 antagonist UBP 302 could significantly reduce the KA EPSCs. These data suggest that both GluK1 and GluK2 play functional roles in the IC. Our study may provide the synaptic basis for the physiology and pathology of KA receptors in the IC-related functions.

Hippocampal Interneurons Are Excited Via Serotonin-Gated Ion Channels

1997 ◽  
Vol 78 (5) ◽  
pp. 2493-2502 ◽  
Author(s):  
Lori L. McMahon ◽  
Julie A. Kauer
Keyword(s):  
Ion Channels ◽  
Synaptic Transmission ◽  
Dentate Gyrus ◽  
Granule Cells ◽  
Brain Slices ◽  
Pyramidal Cells ◽  
Stratum Radiatum ◽  
Negative Slope ◽  
Patch Clamp Recording ◽  
Gated Ion Channels

McMahon, Lori L. and Julie A. Kauer. Hippocampal interneurons are excited via serotonin-gated ion channels. J. Neurophysiol. 78: 2493–2502, 1997. Serotonergic neurons of the median raphe nucleus heavily innervate hippocampal GABAergic interneurons located in stratum radiatum of area CA1, suggesting that this strong subcortical projection may modulate interneuron excitability. Using whole cell patch-clamp recording from interneurons in brain slices, we tested the effects of serotonin (5-HT) on the physiological properties of these interneurons. Serotonin produces a rapid inward current that persists when synaptic transmission is blocked by tetrodotoxin and cobalt, and is unaffected by ionotropic glutamate and γ-aminobutyric acid (GABA) receptor antagonists. The 5-HT–induced current was independent of G-protein activation. Pharmacological evidence indicates that 5-HT directly excites these interneurons through activation of 5-HT3 receptors. At membrane potentials negative to −55 mV, the current-voltage ( I-V) relationship of the 5-HT current displays a region of negative slope conductance. Therefore the response of interneurons to 5-HT strongly depends on membrane potential and increases greatly as cells are depolarized. Removal of extracellular calcium, but not magnesium, increases the amplitude of 5-HT–induced currents and removes the region of negative slope conductance, thereby linearizing the I-V relationship. The axons of 5-HT–responsive interneurons ramify widely within CA1; some of these interneurons also project to and arborize extensively in the dentate gyrus. The organization of these inhibitory connections strongly suggests that these cells regulate excitability of both CA1 pyramidal cells and dentate granule cells. As our results indicate that 5-HT may mediate fast excitatory synaptic transmission onto these interneurons, serotonergic inputs can simultaneously modulate the output of both hippocampus and dentate gyrus.

Glutamatergic Synaptic Plasticity in the Periaqueductal Gray Governs Fear-induced Depression-like Behavior in Rats

2017 ◽  
Vol 41 (S1) ◽  
pp. S633-S633 ◽  
Author(s):  
Y.C. Ho ◽  
M.C. Hsieh ◽  
C.Y. Lai ◽  
H.Y. Peng
Keyword(s):  
Synaptic Transmission ◽  
Learned Helplessness ◽  
Depressive Disorders ◽  
Glutamate Release ◽  
Brain Slices ◽  
Periaqueductal Gray ◽  
Control Group ◽  
Patch Clamp Recording ◽  
Whole Cell Patch Clamp ◽  
Competing Interest

IntroductionMajor depressive disorder affecting more than 110 million people worldwide every year is a heterogeneous illness influenced by a variety of factors, including repeated stressful factors. Despite widely research during the past several decades, the pathophysiology and neurobiological mechanisms of depressive disorders remain unclear. Ventrolateral periaqueductal gray (vlPAG), a midbrain nucleus, has been considered as an important part of the circuitry that involves in stress-induced depression-like behaviors. Dysregulation of glutamatergic neurotransmission in depressed patients suggests that glutamate-mediated excitatory system is critical involved in the depressive disorders.ObjectivesIt is still unclear that whether vlPAG involves in fear condition-elicited depression-like behavior.AimsWe investigated the synaptic transmission in the vlPAG to examine whether vlPAG participates in fear-induced depression-like behavior in rats.MethodsDepression-like behaviors, in the rats, were induced by learned helplessness procedure. The synaptic transmission was conducted by whole-cell patch-clamp recording in the rat brain slices containing periaqueductal gray.ResultsRats receiving learned helplessness procedure displayed high failure rate in the escapable foot-shock test compared to control group. Both amplitude and frequency of miniature excitatory postsynaptic currents were significant reduced compared to control group, suggesting reduced presynaptic glutamate release and postsynaptic responses were involved in the learned helplessness procedure-induced depression behavior in rats.ConclusionsReduced glutamatergic transmission in the vlPAG contributes to learned helplessness procedure-induced depression-like behavior in rats through pre – and post-synaptic mechanisms.Disclosure of interestThe authors have not supplied their declaration of competing interest.

scholarly journals Nicotine Exposure during Adolescence Leads to Changes of Synaptic Plasticity and Intrinsic Excitability of Mice Insular Pyramidal Cells at Later Life

2021 ◽  
Vol 23 (1) ◽  
pp. 34
Author(s):  
Hiroki Toyoda ◽  
Kohei Koga
Keyword(s):  
Synaptic Transmission ◽  
Insular Cortex ◽  
Pyramidal Cells ◽  
Later Life ◽  
Brain Regions ◽  
Spike Timing ◽  
Intrinsic Excitability ◽  
Nicotine Exposure ◽  
Cellular Mechanisms ◽  
Layer V

To find satisfactory treatment for nicotine addiction, synaptic and cellular mechanisms should be investigated comprehensively. Synaptic transmission, plasticity and intrinsic excitability in various brain regions are known to be altered by acute nicotine exposure. However, it has not been addressed whether and how nicotine exposure during adolescence alters these synaptic events and intrinsic excitability in the insular cortex in adulthood. To address this question, we performed whole-cell patch-clamp recordings to examine the effects of adolescent nicotine exposure on synaptic transmission, plasticity and intrinsic excitability in layer V pyramidal neurons (PNs) of the mice insular cortex five weeks after the treatment. We found that excitatory synaptic transmission and potentiation were enhanced in these neurons. Following adolescent nicotine exposure, insular layer V PNs displayed enhanced intrinsic excitability, which was reflected in changes in relationship between current strength and spike number, inter-spike interval, spike current threshold and refractory period. In addition, spike-timing precision evaluated by standard deviation of spike timing was decreased following nicotine exposure. Our data indicate that adolescent nicotine exposure enhances synaptic transmission, plasticity and intrinsic excitability in layer V PNs of the mice insular cortex at later life, which might contribute to severe nicotine dependence in adulthood.

Distinct Local Circuits Between Neocortical Pyramidal Cells and Fast-Spiking Interneurons in Young Adult Rats

2003 ◽  
Vol 89 (2) ◽  
pp. 943-953 ◽  
Author(s):  
María Cecilia Angulo ◽  
Jochen F. Staiger ◽  
Jean Rossier ◽  
Etienne Audinat
Keyword(s):  
Young Adult ◽  
Dendritic Tree ◽  
Release Site ◽  
Pyramidal Cells ◽  
Inhibitory Effect ◽  
Adult Rats ◽  
Release Probability ◽  
Fast Spiking ◽  
Layer V ◽  
Local Circuits

Connections between layer V pyramidal cells and GABAergic fast-spiking interneurons (pyramidal-FS) were studied by paired recordings combined with morphological analyses in acute neocortical slices from 28- to 52-day-old rats. Pairs of spikes elicited in pyramidal cells at a stimulation rate of 0.2 Hz induced unitary excitatory postsynaptic currents (EPSCs) in FS interneurons that displayed facilitation (48%), depression (38.5%), or neither depression nor facilitation (13.5%). Analyses of the EPSC amplitude distributions indicate that depressing connections always showed multiple functional release sites. On the contrary, facilitating connections consisted either of one or several release sites. At a holding potential of −72 mV, the quantal size ( q) and the release probability ( p) of facilitating connections with a single release site were –21.9 ± 7.5 pA and 0.49 ± 0.19 (SD), respectively. The mean q and the estimated number of release sites ( n) at connections showing multiple sites were obtained by decreasing the release probability and did not differ between depressing and facilitating synapses (depressing connections: q = –15.3 ± 2.5 pA, n = 5.1 ± 3, facilitating connections: q = –23.9 ± 9.8 pA, n = 7.8 ± 5.4). However, the quantal content at facilitating synapses with multiple sites (1.9 ± 1.5) was significantly different from that at depressing connections (4.1 ± 3.9). Finally, quantitative morphological analyses revealed that most of the pyramidal cells displaying facilitation can be differentiated from those displaying depression by a more densely branched apical dendritic tree. Therefore two types of morphologically distinct pyramidal cells form excitatory connections with FS interneurons that differ in their short-term plasticity characteristics. Facilitating and depressing connections may provide a differential control of the temporal information processing of FS cells and thus finely regulate the inhibitory effect of these interneurons in neocortical networks of young adult rats.

Cotransmission of GABA and Glycine to Brain Stem Motoneurons

1999 ◽  
Vol 82 (3) ◽  
pp. 1638-1641 ◽  
Author(s):  
Jennifer A. O’Brien ◽  
Albert J. Berger
Keyword(s):  
Brain Stem ◽  
Glycine Receptor ◽  
Aminobutyric Acid ◽  
Decay Kinetics ◽  
Patch Clamp Recording ◽  
Slice Preparation ◽  
Synaptic Inputs ◽  
Whole Cell Patch Clamp ◽  
Presynaptic Vesicle ◽  
Kinetics Of

Using whole cell patch-clamp recording in a rat brain stem slice preparation, we found that γ-aminobutyric acid (GABA) and glycine act as cotransmitters to hypoglossal motoneurons (HMs). Focal application of GABA and glycine onto a single HM revealed that GABAAand glycine receptors are present on the same neuron. To demonstrate that HMs receive both GABAergic and glycinergic synaptic inputs, we simultaneously recorded GABAA- and glycine-receptor–mediated spontaneous miniature inhibitory postsynaptic currents (mIPSCs) in single HMs. GABAergic and glycinergic mIPSCs were differentiated based on their kinetics and modulation by pentobarbital. Specifically, GABAA-receptor–mediated events decayed more slowly than glycine-receptor–mediated events. GABAergic response decay kinetics were prolonged by pentobarbital, whereas glycinergic response decay kinetics remained unchanged. The distinct kinetics of the glycine- and GABAA-receptor-mediated synaptic events allowed us to record dual component mIPSCs, mIPSCs that are mediated by both receptor types. These data suggest that GABA and glycine are colocalized in the same presynaptic vesicle and are coreleased from presynaptic terminals opposed to motoneurons.

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