Retrograde signalling with nitric oxide at neocortical synapses

Volgushev, Maxim; Balaban, P. M.; Chistiakova, Marina; Eysel, Ulf T.

doi:10.1046/j.0953-816x.2000.01322.x

Cited by 54 publications

(86 citation statements)

References 89 publications

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“…The first concerns the fact that, in wild types, synapses are a heterogeneous population, some showing more presynaptic LTP than others. This has been commented on by Volgushev et al (2000) in visual cortex who found that synapses showing high levels of initial paired-pulse ratio were more likely to potentiate than those showing low levels of PPR. We reproduced this result for the GluR1 knock-outs in the barrel cortex (Fig.…”

Section: Discussionmentioning

confidence: 92%

“…However, there has been consistent evidence for a presynaptic component to plasticity in the neocortex from several groups over many years (Markram and Tsodyks, 1996;Sjostrom et al, 2003) and specific evidence that nitric oxide might be involved (Haul et al, 1999;Volgushev et al, 2000). A number of factors may have hampered experimenters from obtaining unambiguous results in the past.…”

Section: Discussionmentioning

confidence: 99%

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The Role of Nitric Oxide and GluR1 in Presynaptic and Postsynaptic Components of Neocortical Potentiation

2006

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In this study, we investigated the mechanisms underlying synaptic plasticity at the layer IV to II/III pathway in barrel cortex of mice aged 6 -13 weeks. This pathway is one of the likely candidates for expression of experience-dependent plasticity in the barrel cortex and may serve as a model for other IV to II/III synapses in the neocortex. We found that postsynaptic autocamtide-2-inhibitory peptide is sufficient to block long-term potentiation (LTP) (IC 50 of 500 nM), implicating postsynaptic calcium/calmodulin-dependent kinase II in LTP induction. AMPA receptor subunit 1 (GluR1) knock-out mice also showed LTP in this pathway, but potentiation was predominantly presynaptic in origin as determined by paired-pulse analysis, coefficient of variation analysis, and quantal analysis, whereas wild types showed a mixed presynaptic and postsynaptic locus. Quantal analysis at this synapse was validated by measuring uniquantal events in the presence of strontium. The predominantly presynaptic LTP in the GluR1 knock-outs was blocked by postsynaptic antagonism of nitric oxide synthase (NOS), either with intracellular N--nitro-L-arginine methyl ester or N-nitro-L-arginine, providing the first evidence for a retrograde transmitter role for NO at this synapse. Antagonism of NOS in wild types significantly reduced but did not eliminate LTP (group average reduction of 50%). The residual LTP formed a variable proportion of the total LTP in each cell and was found to be postsynaptic in origin. We found no evidence for silent synapses in this pathway at this age. Finally, application of NO via a donor induced potentiation in layer II/III cells and caused an increase in frequency but not amplitude of miniature EPSPs, again implicating NO in presynaptic plasticity.

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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 99%

The Role of Nitric Oxide and GluR1 in Presynaptic and Postsynaptic Components of Neocortical Potentiation

2006

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“…Candidate molecules fulfilling the criteria of a retrograde messenger are arachidonic acid, nitric oxide (NO), and carbon monoxide. An involvement of NO in the generation of LTP has been shown for the hippocampus (Zhuo et al, 1993;O'Dell et al, 1994;Arancio et al, 1996) as well as the neocortex (Haul et al, 1999;Volgushev et al, 2000). Mediated by a retrograde messenger, presynaptic LTP should result from an enhanced release of neurotransmitter.…”

Section: Discussionmentioning

confidence: 99%

“…It has been shown that hippocampal LTP is accompanied by an enhanced transmitter release (Malgaroli et al, 1995;Zakharenko et al, 2001). Furthermore, there is evidence for an involvement of retrograde messengers (Bliss and Collingridge, 1993;Volgushev et al, 2000) and presynaptic second messengers (Arancio et al, 1995) in the expression of LTP. Thus, the question of the locus of LTP and LTD has not yet been answered.…”

Section: Abstract: Caged Compounds; Expression Site; Ltp; Ltd; Neocomentioning

confidence: 99%

Neocortical Long-Term Potentiation and Long-Term Depression: Site of Expression Investigated by Infrared-Guided Laser Stimulation

2002

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The synaptic site of expression of long-term potentiation (LTP) and long-term depression (LTD) is still a matter of debate. To address the question of presynaptic versus postsynaptic expression of neocortical LTP and LTD in a direct approach, we measured the glutamate sensitivity of apical dendrites of layer 5 pyramidal neurons during LTP and LTD. We used infraredguided laser stimulation to release glutamate from its "caged" form with high spatial and temporal resolution. Responses to photolytically released glutamate and synaptically evoked EPSPs were recorded with patch-clamp pipettes from the neuronal somata. LTP and LTD could be induced by electrical stimulation at the same synapses in succession. The NMDA receptor-dependent LTD was accompanied by a decrease in the dendritic glutamate sensitivity, suggesting a postsynaptic expression of neocortical LTD. In contrast, LTP was never accompanied by a change in the dendritic glutamate sensitivity. A possible explanation for this finding is a presynaptic expression of neocortical LTP. Another set of experiments corroborated these results: Photolytic application of glutamate with a frequency of 5 Hz caused a long-lasting Ca 2ϩ and NMDA receptor-dependent decrease in the dendritic glutamate sensitivity. In contrast, LTP of dendritic glutamate sensitivity was never induced by photostimulation, despite several experimental modifications to prevent washout of the induction mechanism and to induce a stronger postsynaptic Ca 2ϩ influx. In conclusion, our findings provide strong evidence for a postsynaptic expression of neocortical LTD and favor a primarily presynaptic locus of neocortical LTP. Key words: caged compounds; expression site; LTP; LTD; neocortex; photostimulationLong-term potentiation (LTP) and long-term depression (LTD) of glutamatergic synapses are considered cellular correlates for learning and memory. The molecular mechanisms that underlie the induction and expression of LTP and LTD have been investigated extensively, primarily in the hippocampus. Most of the available evidence speaks in favor of a postsynaptic induction of LTP and LTD by a rise in the intracellular Ca 2ϩ concentration. However, the synaptic site of expression of LTP and LTD is still a matter of debate.Evidence for a postsynaptic expression of LTP and LTD is provided by several observations. (1) The amplitude of miniature EPSCs (mEPSCs) is increased (decreased) during LTP (LTD) (Manabe et al., 1992;Oliet et al., 1996). (2) Hippocampal LTP (LTD) is accompanied by a higher (lower) sensitivity of the postsynaptic membrane for exogenously applied agonists (Davies et al., 1989;Kandler et al., 1998). (3) A synaptic insertion (redistribution) of AMPA receptors occurs after the induction of LTP (LTD) (Liao et al

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“…Our findings are in line with the results by Liu et al (2003) showing that LTP in the visual cortex was completely blocked by a cGMP kinase inhibitor, which itself did not affect basal synaptic transmission. Also, Volgushev et al (2000) reported retrograde signaling of NO to be involved in LTP measured in the visual cortex. The involvement of NO in cortical LTP is further supported by a loss of neocortical LTP in eNOS-deficient mice (Haul et al, 1999) and by an NO-dependent component of LTP found in the barrel cortex (Hardingham and Fox, 2006), in the medial frontal cortex (Nowicky and Bindman, 1993), and in the rat auditory cortex (Wakatsuki et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

Long-Term Potentiation in the Visual Cortex Requires Both Nitric Oxide Receptor Guanylyl Cyclases

Haghikia¹,

Mergia²,

Friebe³

et al. 2007

J. Neurosci.

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The role of nitric oxide (NO)/cGMP signaling in long-term potentiation (LTP) has been a lingering matter of debate. Within the cascade, the NO receptor guanylyl cyclase (GC), the cGMP-forming enzyme that is stimulated by NO, plays a key role. Two isoforms of GC (␣ 2 -GC, ␣ 1 -GC) exist. To evaluate their contribution to synaptic plasticity, we analyzed knock-out mice lacking either one of the GC isoforms. We found that LTP induced in the visual cortex is NO dependent in the wild-type mice, absent in either of the GC isoform-deficient mice, and restored with application of a cGMP analog in both strains. The requirement of both NO receptor GCs for LTP indicates the existence of two distinct NO/cGMP-mediated pathways, which have to work in concert for expression of LTP.

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Retrograde signalling with nitric oxide at neocortical synapses

Cited by 54 publications

References 89 publications

The Role of Nitric Oxide and GluR1 in Presynaptic and Postsynaptic Components of Neocortical Potentiation

The Role of Nitric Oxide and GluR1 in Presynaptic and Postsynaptic Components of Neocortical Potentiation

Neocortical Long-Term Potentiation and Long-Term Depression: Site of Expression Investigated by Infrared-Guided Laser Stimulation

Long-Term Potentiation in the Visual Cortex Requires Both Nitric Oxide Receptor Guanylyl Cyclases

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