Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex

Galarreta, Mario; Hestrin, Shaul

doi:10.1038/2822

Cited by 348 publications

(290 citation statements)

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“…It should be pointed out, however, that the removal of facilitation would work only as long as the incoming Ca 2ϩ does not saturate PV. Thus, for prolonged bursts at high rates of firing, presynaptic Ca 2ϩ accumulation and postsynaptic facilitation are expected to reappear (12), unless depression takes the lead (17,37).…”

Section: Discussionmentioning

confidence: 99%

Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity

Caillard

Moreno

Schwaller

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

373

273

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GABAergic (GABA ‫؍‬ ␥-aminobutyric acid) neurons from different brain regions contain high levels of parvalbumin, both in their soma and in their neurites. Parvalbumin is a slow Ca 2؉ buffer that may affect the amplitude and time course of intracellular Ca 2؉ transients in terminals after an action potential, and hence may regulate short-term synaptic plasticity. To test this possibility, we have applied paired-pulse stimulations (with 30-to 300-ms intervals) at GABAergic synapses between interneurons and Purkinje cells, both in wild-type (PV؉͞؉) mice and in parvalbumin knockout (PV؊͞؊) mice. We observed pairedpulse depression in PV؉͞؉ mice, but paired-pulse facilitation in PV؊͞؊ mice. In paired recordings of connected interneuronPurkinje cells, dialysis of the presynaptic interneuron with the slow Ca 2؉ buffer EGTA (1 mM) rescues paired-pulse depression in PV؊͞؊ mice. These data show that parvalbumin potently modulates short-term synaptic plasticity.GABA ͉ cerebellum ͉ basket cells ͉ stellate cells ͉ Purkinje cells T he immediate consequences of past neuronal activity on synaptic strength are often examined by measuring the ratio (called paired-pulse ratio, or PPR) between the mean synaptic current in response to a test stimulation over that obtained with a conditioning stimulus. If the PPR is larger than 1, the synapse is considered as facilitating, whereas values smaller than 1 are characteristic of depressing synapses. However, facilitation and depression presumably coexist in all experimental conditions, and the PPR that is measured may be viewed as a balance between these two competing processes (1, 2).Current hypotheses link facilitation to the fact that some of the Ca 2ϩ ions entering the presynaptic terminal during the first stimulus are still present when the second stimulus is delivered (3, 4). Several modes of action have been envisaged for the residual calcium. It could act by binding to high affinity sites of the normal exocytosis machinery (5), by binding to special sites responsible for facilitation (2, 6), or by modulating the degree of saturation of high affinity Ca 2ϩ buffers (7, 8), but direct evidence in favor of any of these possibilities is still lacking.Depression is a complex phenomenon including both pre-and postsynaptic components. It may involve depletion of a readily releasable pool of vesicles, saturation or desensitization of postsynaptic receptors, or still other processes (7, 9).Calcium-binding proteins such as parvalbumin (PV), calretinin, and calbindin D 28k are important modulators of intracellular calcium dynamics in neurons (10) and could therefore influence both facilitation and depression. Effects of these calcium buffers are determined by their affinities for Ca 2ϩ ions and by the kinetics (on and off rates) of binding and releasing of Ca 2ϩ . PV is in this regard interesting because it has a slow dissociation rate (about 1 s Ϫ1 ) and a slow apparent association rate (about 10 7 M Ϫ1 ⅐s Ϫ1 ), due to the fact that Mg 2ϩ ions compete with Ca 2ϩ ions for binding. As a result...

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Section: Discussionmentioning

confidence: 99%

Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity

Caillard

Moreno

Schwaller

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

373

273

View full text Add to dashboard Cite

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“…Feedback inhibition via GABAergic interneurons provides a stabilizing influence and prevents runaway excitation (Galarreta and Hestrin, 1998;Varela et al, 1999). It is well established that cortical networks are modulated via dopaminergic (Bjorklund and Lindvall, 1984), noradrenergic (Kawaguchi and Shindou, 1998) and cholinergic (Mesulam et al, 1983) inputs.…”

Section: Introductionmentioning

confidence: 99%

Calcium release via activation of presynaptic IP3 receptors contributes to kainate-induced IPSC facilitation in rat neocortex

Mathew

Hablitz

2008

Neuropharmacology

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We examined the mechanisms of kainate (KA) induced modulation of GABA release in rat prefrontal cortex. Pharmacologically isolated IPSCs were recorded from visually identified layer II/III pyramidal cells using whole cell patch clamp techniques. KA produced an increase in evoked IPSC amplitude at low nanomolar concentrations (100-500 nM). The frequency but not the amplitude of miniature (m) IPSCs was also increased. The GluR5 subunit selective agonist (RS)-2-amino-3-(3-hydroxy-5-tert-butylisoxazol-4-yl) propanoic acid (ATPA) caused an increase in mIPSC frequency whereas (3S,4aR,6S,8aR)-6-(4-carboxyphenyl)methyl-1,2,3,4,4a,5,6,7,8,8a-decahydroisoquinoline-3-carboxylic acid (LY382884), a selective GluR5 subunit antagonist, inhibited this facilitation. Philanthotoxin-433 (PhTx) blocked the effect of KA, indicating involvement of Ca 2+ -permeable GluR5 receptors. No IPSC facilitation was seen when Ca 2+ was omitted from the bathing solution. Facilitation was observed when slices were preincubated in ruthenium red or high concentrations of ryanodine, but was inhibited with application of thapsigargin. The IP3 receptor (IP3R) antagonists diphenylboric acid 2-amino-ethyl ester (2-APB) (15 µM) and Xestospongin C (XeC) blocked IPSC facilitation. These results show that activation of KA receptors (KARs) on GABAergic nerve terminals results is linked to intracellular Ca 2+ release via activation of IP3, but not ryanodine, receptors. This represents a new mechanism of presynaptic modulation whereby Ca 2+ entry thru Ca 2+ -permeable GluR5 subunit containing KARs activates IP3Rs receptors leading to an increase in GABA release.

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“…We limited the trains to 10 -20 pulses to minimize the contribution of post-tetanic potentiation (Magleby, 1987), long-term potentiation (Salin et al, 1996), and a slow form of synaptic depression (Dittman and Regehr, 1998;Galarreta and Hestrin, 1998). The parallel fiber responses exhibited sustained facilitation of neurotransmitter release in response to trains of 10 stimuli (Fig.…”

Section: Use-dependent Plasticity During Trainsmentioning

confidence: 99%

Modulation of Transmission during Trains at a Cerebellar Synapse

Kreitzer

Regehr

2000

J. Neurosci.

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Activity-dependent processes dynamically regulate synapses on the time scale of milliseconds to seconds. Here, we examine the factors governing synaptic strength during repetitive stimulation, both in control conditions and during presynaptic inhibition. Field recordings of presynaptic volleys, optical measurements of presynaptic calcium, and voltage-clamp recordings of postsynaptic currents were used to examine parallel fiber to Purkinje cell synapses in cerebellar brain slices at 34°C. In control conditions, regular stimulus trains (1-50 Hz) evoked up to a 250% peak synaptic enhancement, whereas during irregular stimulation, a threefold variability in EPSC amplitude was observed. When initial EPSC amplitudes were reduced by 50%, either by lowering external calcium or by activating adenosine A 1 or GABA B receptors, the peak enhancement during regular trains was 500%, and synaptic variability during irregular trains was nearly sixfold. By contrast, changes in fiber excitability and calcium influx per pulse were small during trains. Presynaptic calcium measurements indicated that by pulse 10, stimulusevoked calcium influx had increased by ϳ15%, which on the basis of the measured relationship between calcium influx and release corresponds to an EPSC enhancement of 50%. This enhancement was the same in all experimental conditions, even in the presence of N 6 -cyclopentyladenosine or baclofen, suggesting that repetitive stimulation does not relieve the G-protein inhibition of calcium channels by these modulators. Therefore, for our experimental conditions, changes in synaptic strength during trains are primarily attributable to residual calcium (Ca res )-dependent short-term plasticities, and the actions of neuromodulators during repetitive stimulation result from their inhibition of initial calcium influx and the resulting effects on Ca res and calcium-driven processes.

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Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex

Cited by 348 publications

References 50 publications

Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity

Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity

Calcium release via activation of presynaptic IP3 receptors contributes to kainate-induced IPSC facilitation in rat neocortex

Modulation of Transmission during Trains at a Cerebellar Synapse

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