Muscarinic activation reduces changes in [Ca2+]0 evoked by stimulation of Schaffer collaterals during blocked synaptic transmission in rat hippocampal slices

Largo, Carlota, Geoffrey C. Tombaugh, Peter G. Aitken, Oscar Herreras, and George G. Somjen. Heptanol but not fluoroacetate prevents the propagation of spreading depression in rat hippocampal slices. J. Neurophysiol. 77: 9–16, 1997. We investigated whether heptanol and other long-chain alcohols that are known to block gap junctions interfere with the generation or the propagation of spreading depression (SD). Waves of SD were triggered by micro-injection of concentrated KCl solution in stratum (s.) radiatum of CA1 of rat hippocampal tissue slices. DC-coupled recordings of extracellular potential ( V o) were made at the injection and at a second site ∼1 mm distant in st. radiatum and sometimes also in st. pyramidale. Extracellular excitatory postsynaptic potentials (fEPSPs) were evoked by stimulation of the Schaffer collateral bundle; in some experiments, antidromic population spikes were evoked by stimulation of the alveus. Bath application of 3 mM heptanol or 5 mM hexanol completely and reversibly prevented the propagation of the SD-related potential shift (Δ V o) without abolishing the Δ V o at the injection site. Octanol (1 mM) had a similar but less reliably reversible effect. fEPSPs were depressed by ∼30% by heptanol and octanol, 65% by hexanol. Antidromic population spikes were depressed by 30%. In isolated, patch-clamped CA1 pyramidal neurons, heptanol partially and reversibly depressed voltage-dependent Na currents possibly explaining the slight depression of antidromic spikes and, by acting on presynaptic action potentials, also the depression of fEPSPs. Fluoroacetate (FAc), a putative selective blocker of glial metabolism, first induced multiple spike firing in response to single afferent volleys and then severely suppressed synaptic transmission (confirming earlier reports) without depressing the antidromic population spike. FAc did not inhibit SD propagation. The effect of alkyl alcohols is compatible with the idea that the opening of normally closed neuronal gap junctions is required for SD propagation. Alternative possible explanations include interference with the lipid phase of neuron membranes. The absence of SD inhibition by FAc confirms that synaptic transmission is not necessary for the propagation of SD, and it suggests that normally functioning glial cells are not essential for SD generation or propagation.

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Hyperoxic stimulation of synchronous orthodromic activity and induction of neural plasticity does not require changes in excitatory synaptic transmission

Journal of Applied Physiology ◽

10.1152/japplphysiol.91430.2008 ◽

2010 ◽

Vol 109 (3) ◽

pp. 820-829 ◽

Cited By ~ 5

Author(s):

Alfredo J. Garcia ◽

Robert W. Putnam ◽

Jay B. Dean

Keyword(s):

Synaptic Transmission ◽

Epileptiform Activity ◽

Hippocampal Slices ◽

Field Potential ◽

Excitatory Synaptic Transmission ◽

Population Spike ◽

Excitatory Postsynaptic Potential ◽

Synaptic Activation ◽

Ca1 Neurons ◽

Stimulation Of

The first study, described in the companion article, reports that acute exposure of rat hippocampal slices to either hyperbaric oxygen (HBO: 2.84 and 4.54 atmospheres absolute, ATA) or normobaric reoxygenation (NBOreox; i.e., normobaric hyperoxia: 0.6 or 0.0 → 0.95 ATA) stimulates synchronous orthodromic activity in CA1 neurons, which includes activation of O2-induced potentiation (OxIP) and, in some cases, hyperexcitability (secondary population spikes, sPS). In this second study we tested the hypothesis that HBO and NBOreox increase orthodromic activity of CA1 neurons (oPS, orthodromic population spike) and OxIP via a combination of both increased excitatory synaptic transmission (field excitatory postsynaptic potential, fEPSP) and intrinsic excitability (antidromic population spike, aPS). HBO and NBOreox increased the oPS but rarely increased or potentiated the fEPSP. HBO exposure produced epileptiform antidromic activity, which was abolished during inhibition of fast GABAergic and glutamatergic synaptic transmission. Decreasing O2 from 0.95 ATA (control) to 0.6 ATA (intermediate O2) or 0.0 ATA (hypoxia) reversibly abolished the fEPSP, and reoxygenation rarely induced potentiation of the fEPSP or aPS. Intracellular recordings and antidromic field potential recordings, however, revealed that synaptic transmission and neuronal excitability were preserved, albeit at lower levels, in 0.60 ATA O2. Together, these data indicate that 1) the changes in excitatory postsynaptic activity are not required for stimulation of the oPS during and HBO/NBOreox or for activation of OxIP, suggesting the latter is a form of intrinsic plasticity; 2) HBO disinhibits spontaneous synaptic transmission to induce epileptiform activity; and 3) although synchronous synaptic activation of the CA1 neuronal population requires hyperoxia (i.e., 0.95 ATA O2), synaptic activation of individual CA1 neurons does not.

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Relative contributions of excitatory and inhibitory neuronal activity to alkaline transients evoked by stimulation of Schaffer collaterals in the rat hippocampal slice

Journal of Neurophysiology ◽

10.1152/jn.1995.74.2.643 ◽

1995 ◽

Vol 74 (2) ◽

pp. 643-649 ◽

Cited By ~ 21

Author(s):

T. Taira ◽

P. Paalasmaa ◽

J. Voipio ◽

K. Kaila

Keyword(s):

Hippocampal Slices ◽

Low Frequency ◽

Gamma Aminobutyric Acid ◽

Schaffer Collaterals ◽

Stratum Pyramidale ◽

Low Frequency Stimulation ◽

S 100 ◽

Drug Inhibition ◽

Frequency Stimulation ◽

Stimulation Of

1. The neuronal basis of alkaline shifts in extracellular pH (pHo) evoked by stimulation of Schaffer collaterals was studied by means of double-barreled H(+)-selective microelectrodes in the area CA1 of rat hippocampal slices. 2. Alkaline transients in stratum pyramidale evoked by stimulation at a low frequency (5–10 Hz) were enhanced by pentobarbital sodium (100 microM). In the absence of the drug, inhibition of extracellular carbonic anhydrase (CAo) by benzolamide or by prontosildextran 5000 (PD 5000) resulted in an increase in the alkaline shifts. In contrast to this, alkaloses evoked by low-frequency stimulation in the presence of pentobarbital were attenuated by a subsequent inhibition of CAo. 3. Blockade of gamma-aminobutyric acid-A (GABAA) receptors with picrotoxin (PiTX; 100 microM) resulted in an enhancement of alkaline transients in s. pyramidale evoked by low-frequency stimulation (10 Hz) but suppressed alkaline shifts evoked by brief high-frequency (1 s, 100 Hz) trains of stimuli. 4. Application of trains of stimuli consisting of a constant number of pulses (50 or 100) revealed a striking dependence of the effect of benzolamide on stimulation frequency (10-200 Hz) in s. pyramidale: the enhancement of the alkaloses seen upon inhibition of CAo became progressively smaller with an increase in frequency, and at 100-200 Hz benzolamide produced a suppression or a complete block of the alkaline transients. However, alkaline transients evoked with the use of a constant train duration (5 s) were enhanced by benzolamide at all stimulation frequencies examined (5–200 Hz).(ABSTRACT TRUNCATED AT 250 WORDS)

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Glycolysis Prevents Anoxia-Induced Synaptic Transmission Damage in Rat Hippocampal Slices

Journal of Neurophysiology ◽

10.1152/jn.2000.83.4.1830 ◽

2000 ◽

Vol 83 (4) ◽

pp. 1830-1839 ◽

Cited By ~ 34

Author(s):

Guo-Feng Tian ◽

Andrew J. Baker

Keyword(s):

Synaptic Transmission ◽

Anaerobic Metabolism ◽

Cell Layer ◽

Hippocampal Slices ◽

Sodium Cyanide ◽

Artificial Cerebrospinal Fluid ◽

Elevated Glucose ◽

Chemical Anoxia ◽

Stimulation Of

Prolonged anoxia can cause permanent damage to synaptic transmission in the mammalian CNS. We tested the hypothesis that lack of glucose is the major cause of irreversible anoxic transmission damage, and that anoxic synaptic transmission damage could be prevented by glycolysis in rat hippocampal slices. The evoked population spike (PS) was extracellularly recorded in the CA1 pyramidal cell layer after stimulation of the Schaffer collaterals. When the slice was superfused with artificial cerebrospinal fluid (ACSF) containing 4 mM glucose, following 10 min anoxia, the evoked PS did not recover at all after 60 min reoxygenation. When superfusion ACSF contained 10 mM glucose with or without 0.5 mM α-cyano-4-hydroxycinnate (4-CIN), after 60 min reoxygenation the evoked PS completely recovered following 10 min anoxia. When superfusion ACSF contained 20 mM glucose with or without 1 mM sodium cyanide (NaCN), after 60 min reoxygenation the evoked PS completely recovered even following 120 min anoxia. In contrast, when superfusion ACSF contained 4 mM glucose, following 10 min 1 mM NaCN chemical anoxia alone, without anoxic anoxia, the evoked PS displayed no recovery after 60 min reoxygenation. Moreover, when 16 mM mannitol and 16 sodiuml-lactate were added into 4 mM glucose ACSF, following 10 min anoxia the evoked PS failed to recover at all after 60 min reoxygenation. The results indicate that elevated glucose concentration powerfully protected the synaptic transmission against anoxic damage, and the powerful protection is due to anaerobic metabolism of glucose and not a result of the higher osmolality in higher glucose ACSF. We conclude that lack of glucose is the major cause of anoxia-induced synaptic transmission damage, and that if sufficient glucose is supplied, glycolysis could prevent this damage in vitro.

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EFFECT OF TWO NEW TRIPEPTIDES ON THE HIPPOCAMPUS IN RATS

Aerospace and Environmental Medicine ◽

10.21687/0233-528x-2021-55-4-73-77 ◽

2021 ◽

Vol 55 (4) ◽

pp. 73-77

Author(s):

Vik.V. Yasnetsov ◽

◽

Yu.V. Ivanov ◽

S.K. Karsanova ◽

V.V. Yasnetsov ◽

...

Keyword(s):

Synaptic Transmission ◽

Nmda Receptors ◽

Pyramidal Neurons ◽

Hippocampal Slices ◽

The Other ◽

Short Term ◽

Population Responses ◽

Schaffer Collaterals ◽

Term Potentiation ◽

Field Ca1

Experiments on hippocampal slices in rats showed that, in contrast to piracetam (100 µM to 10 mM), two new tripeptides, i.e. H-asparagil-glutamyl-proline-OH and H-asparagil-glutamyl-arginin-OH (concentrations 500 µM, 1 and 2.5 mM respectively), strengthened the orthodrome population responses in field СА1. In all three concentrations the effect of H-asparagil-glutamyl-proline-OH was stronger than of the other tripeptide. That is both tripeptides facilitate synaptic transmission within the Schaffer collaterals-pyramidal neurons system in hippocumpal field CA1. Similarly to piracetam (100 µM, within 15 minutes) these tripeptides supported short-term potentiation of the hippocampal synaptic transfer by N-methyl-D-aspartate (NMDA). Specific NMDA-receptors antagonist D-AP5 cancelled the NMDA effect fully which infers that the observed effect is achieved through activation of NMDA-receptors. Effect from H-asparagil-glutamyl-proline-OH excelled equally piracetam and H-asparagil-glutamyl-arginin-OH; H-asparagil-glutamyl-arginin-OH excelled piracetam only.

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Pharmacological characterization of extracellular pH transients evoked by selective synaptic and exogenous activation of AMPA, NMDA, and GABAA receptors in the rat hippocampal slice

Journal of Neurophysiology ◽

10.1152/jn.1995.74.2.633 ◽

1995 ◽

Vol 74 (2) ◽

pp. 633-642 ◽

Cited By ~ 24

Author(s):

J. Voipio ◽

P. Paalasmaa ◽

T. Taira ◽

K. Kaila

Keyword(s):

Carbonic Anhydrase ◽

Hippocampal Slices ◽

Extracellular Ph ◽

Stratum Radiatum ◽

Diagnostic Tools ◽

Synaptic Activation ◽

Simultaneous Presence ◽

Glutamate Antagonists ◽

Schaffer Collaterals ◽

Stimulation Of

1. Inhibitors of extracellular carbonic anhydrase (CAo) offer much promise as diagnostic tools in the study of the synaptic basis of activity-induced alkaline transients in the brain. However, most of the present information related to the effects of CAo blockers in nervous tissue comes from experiments that involve simultaneous synaptic activation of various types of postsynaptic receptor channels. In the present work, double-barreled H(+)-selective microelectrodes were used to study alkaline shifts in extracellular pH (pHo) evoked by selective synaptic and pharmacological activation of glutamate and gamma-aminobutyric acid (GABA) receptors in the CA1 cell body layer in rat hippocampal slices. Inhibition of CAo was achieved with the use of the poorly permeant carbonic anhydrase inhibitor, benzolamide (10 microM; applied in the bath solution) or the impermeant macromolecular inhibitor, prontosil-dextran 5000 (PD 5000; applied in microdrops). 2. Alkaline transients that were exclusively attributable to synaptic activation of glutamate receptors were induced by stimulation of Schaffer collaterals in the presence of picrotoxin (PiTX, 100 microM). An enhancement by the CAo inhibitors of these alkaline transients took place at all stimulus frequencies (5–200 Hz) and stimulus train durations (0.5–20 s) examined. 3. Inhibition of CAo enhanced the alkaline transients evoked by selective synaptic activation of alpha-amino-3-hydroxy-5-methyli-oxazolate- 4-propionic acid (AMPA)/kainate receptors in experiments involving stimulation of Schaffer collaterals in the simultaneous presence of PiTX and D-2-amino-5-phosphonopentoate (AP5, 40-80 microM). 4. Alkaline shifts evoked by selective synaptic activation of N-methyl-D-aspartate (NMDA) receptors were enhanced after inhibition of CAo as seen in experiments where Schaffer collaterals were stimulated in the simultaneous presence of PiTX and 6-cyano-2,3-dihydroxy-7-nitroquinoxaline (CNQX, 20–40 microM) in an Mg(2+)-free solution. 5. Benzolamide and PD 5000 also enhanced the alkaline shifts seen upon pressure injection of glutamate, AMPA, or NMDA. The glutamate-induced alkaline shifts were inhibited by AP5+CNQX, suggesting that uptake of glutamate did not significantly contribute to their generation. 6. Stimuli applied at 5–10 Hz in stratum radiatum close (within 0.5 mm) to the recording site evoked alkaline shifts that were blocked by CNQX plus AP5. In the continuous presence of the two glutamate antagonists, PiTX-sensitive alkaline transients were observed in response to brief high-frequency (20–100 Hz) trains consisting of 100 stimuli. Upon application of pentobarbital sodium (100 microM), these apparently monosynaptically evoked GABAA receptor-mediated alkaline transients were evident also at low stimulation frequencies (5–10 Hz).(ABSTRACT TRUNCATED AT 400 WORDS)

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