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.

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.

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.

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.

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.

Novel nootropic dipeptide Noopept increases inhibitory synaptic transmission in CA1 pyramidal cells

2010 ◽  
Vol 476 (2) ◽  
pp. 70-73 ◽  
Author(s):  
Rodion V. Kondratenko ◽  
Vladimir I. Derevyagin ◽  
Vladimir G. Skrebitsky
Keyword(s):  
Synaptic Transmission ◽  
Pyramidal Cells ◽  
Inhibitory Synaptic Transmission ◽  
Ca1 Pyramidal Cells

scholarly journals Cannabinoids Modulate Synaptic Strength and Plasticity at Glutamatergic Synapses of Rat Prefrontal Cortex Pyramidal Neurons

2000 ◽  
Vol 83 (6) ◽  
pp. 3287-3293 ◽  
Author(s):  
Nathalie Auclair ◽  
Satoru Otani ◽  
Philippe Soubrie ◽  
Francis Crepel
Keyword(s):  
Prefrontal Cortex ◽  
Synaptic Transmission ◽  
Cannabinoid Receptors ◽  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Type I ◽  
Glutamatergic Synaptic Transmission ◽  
Layer V ◽  
Stimulation Of

Cannabinoids receptors have been reported to modulate synaptic transmission in many structures of the CNS, but yet little is known about their role in the prefrontal cortex where type I cannabinoid receptor (CB-1) are expressed. In this study, we tested first the acute effects of selective agonists and antagonist of CB-1 on glutamatergic excitatory postsynaptic currents (EPSCs) in slices of rat prefrontal cortex (PFC). EPSCs were evoked in patch-clamped layer V pyramidal cells by stimulation of layer V afferents. Monosynaptic EPSCs were strongly depressed by bath application (1 μM) of the cannabinoid receptors agonists WIN55212-2 (−50.4 ± 8.8%) and CP55940 (−42.4 ± 10.9%). The CB-1 antagonist SR141716A reversed these effects. Unexpectedly, SR141716A alone produced a significant increase of glutamatergic synaptic transmission (+46.9 ± 11.2%), which could be partly reversed by WIN55212-2. In the presence of strontium in the bath, the frequency but not the amplitude of asynchronous synaptic events evoked in layer V pyramidal cells by stimulating layer V afferents, was markedly decreased (−54.2 ± 8%), indicating a presynaptic site of action of cannabinoids at these synapses. Tetanic stimulation (100 pulses at 100 Hz, 4 trains) induced in control condition, no changes ( n = 7/18), long-term depression (LTD; n = 6/18), or long-term potentiation (LTP; n = 5/18) of monosynaptic EPSCs evoked by stimulation of layer V afferents. When tetanus was applied in the presence of WIN 55,212-2 or SR141716-A (1 μM) in the bath, the proportion of “nonplastic” cells were not significantly changed ( n = 7/15 in both cases). For the plastic ones ( n = 8 in both cases), WIN 55,212-2 strongly favored LTD ( n = 7/8) at the apparent expense of LTP ( n = 1/8), whereas the opposite effect was observed with SR141716-A (7/8 LTP; 1/8 LTD). These results demonstrate that cannabinoids influence glutamatergic synaptic transmission and plasticity in the PFC of rodent.

scholarly journals Cell type-specific regulation of inhibition via cannabinoid type 1 receptors in rat neocortex

2013 ◽  
Vol 109 (1) ◽  
pp. 216-224 ◽  
Author(s):  
Claire L. De-May ◽  
Afia B. Ali
Keyword(s):  
Synaptic Transmission ◽  
Pyramidal Cell ◽  
Metabotropic Glutamate Receptor ◽  
Pyramidal Cells ◽  
Cb1 Receptor ◽  
Cb1 Receptors ◽  
Cell Type ◽  
Group I ◽  
Cell Type Specific

Endogenous cannabinoid type 1 (CB1) receptors demonstrate a cell type-specific expression and are potent modulators of synaptic transmission within the central nervous system. We aimed to investigate whether two classes of multipolar interneuron in the neocortex displayed a form of short-term synaptic plasticity, depolarization-induced suppression of inhibition (DSI), and whether the DSI was mediated by a common receptor. Paired whole cell recordings combined with biocytin labeling were performed between pyramidal cells and either multipolar adapting or multipolar nonadapting interneurons in layers II–IV of male Wistar rat (postnatal day 17–22) somatosensory cortex. Inhibitory postsynaptic potentials elicited by multipolar adapting interneurons were sensitive to DSI, which was blocked by the CB1 receptor antagonist AM-251 (8 μM), indicating that the suppression of inhibition was mediated by CB1 receptors. Two subpopulations of multipolar nonadapting interneuron-to-pyramidal cell connections were discovered on the basis of their susceptibility to DSI. Whereas 50% were insensitive to DSI, the remaining half were sensitive to DSI, which could not be prevented by AM-251. DSI at these connections was also insensitive to the group I (mGluRIa) and III metabotropic glutamate receptor antagonists ( RS)-1-aminoindan-1,5-dicarboxylic acid (100 μM) and ( RS)-α-cyclopropyl-4-phosphonophenylglycine (100 μM) and the group III agonist l-2-amino-4-phosphonobutanoate (50 μM). However, multipolar nonadapting interneuron-to-pyramidal cell connections were sensitive to the endocannabinoid anandamide (9 μM), mimicking the effects of DSI, which also could not be prevented by AM-251, implying a CB1 receptor-independent suppression of inhibition. These results reveal an interneuron type-specific modulation of synaptic transmission via CB receptors in the neocortex.

scholarly journals Intranasal Administration of Rotenone Reduces GABAergic Inhibition in the Mouse Insular Cortex Leading to Impairment of LTD and Conditioned Taste Aversion Memory

2020 ◽  
Vol 22 (1) ◽  
pp. 259
Author(s):  
Hiroki Toyoda ◽  
Ayano Katagiri ◽  
Takafumi Kato ◽  
Hajime Sato
Keyword(s):  
Synaptic Transmission ◽  
Taste Aversion ◽  
Conditioned Taste Aversion ◽  
Intranasal Administration ◽  
Pyramidal Neurons ◽  
Insular Cortex ◽  
Long Term Potentiation ◽  
Cellular Mechanisms ◽  
Layer V

The pesticide rotenone inhibits mitochondrial complex I and is thought to cause neurological disorders such as Parkinson’s disease and cognitive disorders. However, little is known about the effects of rotenone on conditioned taste aversion memory. In the present study, we investigated whether intranasal administration of rotenone affects conditioned taste aversion memory in mice. We also examined how the intranasal administration of rotenone modulates synaptic transmission and plasticity in layer V pyramidal neurons of the mouse insular cortex that is critical for conditioned taste aversion memory. We found that the intranasal administration of rotenone impaired conditioned taste aversion memory to bitter taste. Regarding its cellular mechanisms, long-term depression (LTD) but not long-term potentiation (LTP) was impaired in rotenone-treated mice. Furthermore, spontaneous inhibitory synaptic currents and tonic GABA currents were decreased in layer V pyramidal neurons of rotenone-treated mice compared to the control mice. The impaired LTD observed in pyramidal neurons of rotenone-treated mice was restored by a GABAA receptor agonist muscimol. These results suggest that intranasal administration of rotenone decreases GABAergic synaptic transmission in layer V pyramidal neurons of the mouse insular cortex, the result of which leads to impairment of LTD and conditioned taste aversion memory.

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