Effects of changes in extracellular potassium, magnesium and calcium concentration on synaptic transmission in area CA1 and the dentate gyrus of rat hippocampal slices

1990 ◽  
Vol 415 (5) ◽  
pp. 588-593 ◽  
Author(s):  
G. Rausche ◽  
P. Igelmund ◽  
U. Heinemann
Keyword(s):  
Synaptic Transmission ◽  
Dentate Gyrus ◽  
Calcium Concentration ◽  
Hippocampal Slices ◽  
Extracellular Potassium ◽  
Area Ca1 ◽  
Potassium Magnesium

Altered synaptic transmission in dentate gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro

1986 ◽  
Vol 55 (4) ◽  
pp. 739-750 ◽  
Author(s):  
E. J. Green ◽  
W. T. Greenough
Keyword(s):  
Synaptic Transmission ◽  
Dentate Gyrus ◽  
Granule Cell ◽  
Granule Cells ◽  
Cell Layer ◽  
Molecular Layer ◽  
Hippocampal Slices ◽  
Granule Cell Layer ◽  
Complex Environments ◽  
Rearing Environment

Pre- and postsynaptic responses to activation of medial perforant path (MPP) axons were examined in hippocampal slices taken from rats reared for 3-4 wk in relatively complex (EC) or individual cage (IC) environments. Three types of extracellular field potentials were recorded in the infrapyramidal blade of the dentate gyrus: 1) granule cell population spikes (PSs), which reflect the number and synchrony of discharging granule cells (2), 2) population excitatory postsynaptic potentials (EPSPs), which reflect the amount of excitatory synaptic current flow into dendrites (28), and 3) presynaptic fiber volleys (FVs), which reflect the number of activated axons (28). Stimulation of the MPP evoked significantly larger PSs in slices taken from EC rats. There was no significant effect of rearing environment on PS/EPSP relationships. The slopes of EPSPs recorded at the site of synaptic activation in the dentate molecular layer and at the major current source in the dentate granule cell layer were significantly greater in slices taken from EC rats. The presynaptic FV was recorded at the site of synaptic activation in the molecular layer. FV amplitude did not differ significantly as a function of rearing environment. To examine possible differences in tissue impedance, granule cells were activated by stimulating granule cell axons in the dentate hilus and recording the antidromic PS in the granule cell layer. Antidromic PS amplitude was not significantly affected by rearing environment. The relative permanence of the experience-dependent alterations in synaptic transmission was assessed by comparing slices taken from rats that had been reared for 4 wk in complex environments followed by 3-4 wk in individual cages with those from rats reared for 7-8 wk in individual cages. There were no significant differences in MPP synaptic transmission between these groups of animals. The results suggest that experience in a relatively complex environment is associated with greater MPP synaptic transmission arising from an increased synaptic input to granule cells; the greater MPP synaptic transmission associated with behavioral experience can occur independent of behavioral state, influences from extrahippocampal brain regions and intrahippocampal inhibitory activity; and the experience-dependent synaptic alterations in the dentate gyrus are transient, in contrast to experience-dependent morphological alterations described in occipital cortex. The possible relationship of these alterations to the phenomenon of long-term enhancement is discussed.

Cesium Induces Spontaneous Epileptiform Activity Without Changing Extracellular Potassium Regulation in Rat Hippocampus

1999 ◽  
Vol 82 (6) ◽  
pp. 3339-3346 ◽  
Author(s):  
Zhi-Qi Xiong ◽  
Janet L. Stringer
Keyword(s):  
Nmda Receptor ◽  
Dentate Gyrus ◽  
Extracellular Space ◽  
Hippocampal Neurons ◽  
Epileptiform Activity ◽  
Hippocampal Slices ◽  
Nmda Receptor Antagonist ◽  
Extracellular Potassium ◽  
Epileptiform Discharges ◽  
Cultured Hippocampal Neurons

Cesium has been widely used to study the roles of the hyperpolarization-activated (Ih) and inwardly rectifying potassium (KIR) channels in many neuronal and nonneuronal cell types. Recently, extracellular application of cesium has been shown to produce epileptiform activity in brain slices, but the mechanisms for this are not known. It has been proposed that cesium blocks the KIR in glia, resulting in an abnormal accumulation of potassium in the extracellular space and inducing epileptiform activity. This hypothesis has been tested in hippocampal slices and cultured hippocampal neurons using potassium-sensitive microelectrodes. In the present study, application of cesium produced spontaneous epileptiform discharges at physiological extracellular potassium concentration ([K+]o) in the CA1 and CA3 regions of hippocampal slices. This epileptiform activity was not mimicked by increasing the [K+]o. The epileptiform discharges induced by cesium were not blocked by the N-methyl-d- aspartate (NMDA) receptor antagonist AP-5, but were blocked by the non-NMDA receptor antagonist CNQX. In the dentate gyrus, cesium induced the appearance of spontaneous nonsynaptic field bursts in 0 added calcium and 3 mM potassium. Moreover, cesium increased the frequency of field bursts already present. In contrast, ZD-7288, a specific Ihblocker, did not cause spontaneous epileptiform activity in CA1 and CA3, nor did it affect the field bursts in the dentate gyrus, suggesting that cesium induced epileptiform activity is not directly related to blockade of the Ih. When potassium-sensitive microelectrodes were used to measure [K+]o, there was no significant increase in [K+]o in CA1 and CA3 after cesium application. In the dentate gyrus, cesium did not change the baseline level of [K+]o or the rate of [K+]o clearance after the field bursts. In cultured hippocampal neurons, which have a large and relatively unrestricted extracellular space, cesium also produced cellular burst activity without significantly changing the resting membrane potential, which might indicate an increase in [K+]o. Our results suggest that cesium causes epileptiform activity by a mechanism unrelated to an alteration in [K+]o regulation.

Isoproterenol increases the phosphorylation of the synapsins and increases synaptic transmission in dentate gyrus, but not in area CA1, of the hippocampus

Hippocampus ◽  
1992 ◽  
Vol 2 (1) ◽  
pp. 59-64 ◽  
Author(s):  
Karen D. Parfitt ◽  
A. Van Doze ◽  
Daniel V. Madison ◽  
Michael D. Browning
Keyword(s):  
Synaptic Transmission ◽  
Dentate Gyrus ◽  
Area Ca1

Increased propensity for nonsynaptic epileptiform activity in immature rat hippocampus and dentate gyrus

1993 ◽  
Vol 70 (2) ◽  
pp. 857-862 ◽  
Author(s):  
S. N. Roper ◽  
A. Obenaus ◽  
F. E. Dudek
Keyword(s):  
Dentate Gyrus ◽  
Excitatory Amino Acid ◽  
Epileptiform Activity ◽  
Hippocampal Slices ◽  
Age Groups ◽  
Adult Group ◽  
Adult Rats ◽  
Area Ca1 ◽  
Immature Rats ◽  
Old Adult

1. Low-[Ca2+] bursting was studied in hippocampal slices from immature and adult rats to test the hypothesis that the increased seizure susceptibility of the immature brain involves nonsynaptic mechanisms. Extracellular recordings were obtained from area CA1 of the hippocampus and from the dentate gyrus in slices from rats 6-9 days old (1 wk), 11-15 days old (2 wk), 19-23 days old (3 wk), and > 60 days old (adult). These slices were exposed to a low-[Ca2+] solution that included the calcium chelator, ethylene glycol-bis(beta-aminoethyl ether)-N,N,N',N'-tetraacetic acid (EGTA), and the excitatory amino acid antagonists, 6,7-dinitroquinoxaline-2,3-dione (DNQX) and DL-2-amino-5-phosphonopentanoic acid (AP-5). They were also exposed to a hyposmolar low-[Ca2+] solution (diluted with 20% H2O by volume), which induced or intensified the bursting. The propensity for nonsynaptic bursting and the characteristics of the bursts were compared between age groups. 2. The 1-wk group showed no bursting activity under any treatment condition in either CA1 or the dentate gyrus. Bursting occurred more frequently in the 2- and 3-wk groups than in the adult group in both CA1 and the dentate gyrus. 3. In CA1 the duration of the bursts was longer in the 2- and 3-wk groups as compared with the adult group. The number of population spikes per burst was also higher in slices from immature rats in dilute low-[Ca2+] solution. These findings demonstrate that nonsynaptic bursting in area CA1 is more robust in tissue from immature rats than adults.(ABSTRACT TRUNCATED AT 250 WORDS)

Sodium Pump Activity, Not Glial Spatial Buffering, Clears Potassium After Epileptiform Activity Induced in the Dentate Gyrus

2000 ◽  
Vol 83 (3) ◽  
pp. 1443-1451 ◽  
Author(s):  
Zhi-Qi Xiong ◽  
Janet L. Stringer
Keyword(s):  
Dentate Gyrus ◽  
Epileptiform Activity ◽  
Hippocampal Slices ◽  
Local Application ◽  
Minor Role ◽  
Extracellular Potassium ◽  
Half Time ◽  
Atpase Inhibitor ◽  
Adult Rats ◽  
Extracellular Potassium Concentration

A number of mechanisms have been proposed to play a role in the regulation of activity-dependent variations in extracellular potassium concentration ([K+]o). We tested possible regulatory mechanisms for [K+]o during spontaneous recurrent epileptiform activity induced in the dentate gyrus of hippocampal slices from adult rats by perfusion with 8 mM potassium and 0-added calcium medium in an interface chamber. Local application of tetrodotoxin blocked local [K+]o changes, suggesting that potassium is released and taken up locally. Perfusion with barium or cesium, blockers of the inward rectifying potassium channel, did not alter the baseline [K+]o, the ceiling level of [K+]o reached during the burst, or the rate of [K+]o recovery after termination of the bursts. Decreasing gap junctional conductance did not change the baseline [K+]o or the half-time of recovery of the [K+]o after the bursts but did cause a decrease in the ceiling level of [K+]o. Perfusion with furosemide, which will block cation/chloride cotransporters, or perfusion with low chloride did not change the baseline [K+]o or the half-time of recovery of the [K+]o after the bursts but did increase the ceiling level of [K+]o. Bath or local application of ouabain, a Na+/K+-ATPase inhibitor, increased the baseline [K+]o, slowed the rate of [K+]o recovery, and induced spreading depression. These findings suggest that potassium redistribution by glia only plays a minor role in the regulation of [K+]o in this model. The major regulator of [K+]o in this model appears to be uptake via a Na+/K+-ATPase, most likely neuronal.

scholarly journals Activity-Dependent Plasticity of Astroglial Potassium and Glutamate Clearance

2015 ◽  
Vol 2015 ◽  
pp. 1-16 ◽  
Author(s):  
Giselle Cheung ◽  
Jérémie Sibille ◽  
Jonathan Zapata ◽  
Nathalie Rouach
Keyword(s):  
Synaptic Transmission ◽  
Neuronal Activity ◽  
Hippocampal Slices ◽  
Low Frequency ◽  
Extracellular Potassium ◽  
Inward Currents ◽  
Frequency Stimulation ◽  
Short And Long Term ◽  
Acute Hippocampal Slices

Recent evidence has shown that astrocytes play essential roles in synaptic transmission and plasticity. Nevertheless, how neuronal activity alters astroglial functional properties and whether such properties also display specific forms of plasticity still remain elusive. Here, we review research findings supporting this aspect of astrocytes, focusing on their roles in the clearance of extracellular potassium and glutamate, two neuroactive substances promptly released during excitatory synaptic transmission. Their subsequent removal, which is primarily carried out by glial potassium channels and glutamate transporters, is essential for proper functioning of the brain. Similar to neurons, different forms of short- and long-term plasticity in astroglial uptake have been reported. In addition, we also present novel findings showing robust potentiation of astrocytic inward currents in response to repetitive stimulations at mild frequencies, as low as 0.75 Hz, in acute hippocampal slices. Interestingly, neurotransmission was hardly affected at this frequency range, suggesting that astrocytes may be more sensitive to low frequency stimulation and may exhibit stronger plasticity than neurons to prevent hyperexcitability. Taken together, these important findings strongly indicate that astrocytes display both short- and long-term plasticity in their clearance of excess neuroactive substances from the extracellular space, thereby regulating neuronal activity and brain homeostasis.

Role of Potassium and Calcium in the Generation of Cellular Bursts in the Dentate Gyrus

1997 ◽  
Vol 77 (5) ◽  
pp. 2293-2299 ◽  
Author(s):  
Enhui Pan ◽  
Janet L. Stringer
Keyword(s):  
Dentate Gyrus ◽  
Granule Cells ◽  
Seizure Activity ◽  
Epileptiform Activity ◽  
Hippocampal Slices ◽  
Extracellular Potassium ◽  
Sprague Dawley

Pan, Enhui and Janet L. Stringer. Role of potassium and calcium in the generation of cellular bursts in the dentate gyrus. J. Neurophysiol. 77: 2293–2299, 1997. Epileptiform activity, which appears to be endogenous, has been recorded in the granule cells of the dentate gyrus before the onset of synchronized seizure activity and has been termed cellular bursts. It has been postulated that an increase in input to the dentate gyrus causes a local increase in extracellular K+ concentration ([K+]o) and a decrease in [Ca2+]o that results in this cellular bursting. The first test of this hypothesis is to determine whether the cellular bursts appear in ionic conditions that occur in vivo before the onset of synchronized epileptic activity. This hypothesis was tested in vitro by varying the ionic concentrations in the perfusing solution and recording changes in the granule cells of the dentate gyrus. Intra- and extracellular recordings were made in the dentate gyri of hippocampal slices prepared from anesthetized adult Sprague-Dawley rats. Increasing the extracellular potassium or decreasing the extracellular calcium of the perfusing solution caused three forms of spontaneous activity to appear: depolarizing potentials, action potentials, and cellular bursts. Increasing potassium or decreasing calcium also caused the granule cells to depolarize and reduced their input resistance. No synchronized extracellular field activity was detected. Simultaneously increasing potassium and decreasing calcium caused cellular bursts to appear at concentrations recorded in vivo before the onset of synchronized reverberatory seizure activity.

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