Presynaptic mechanism for long-term potentiation in the hippocampus

Bekkers, John M.; Stevens, Charles F.

doi:10.1038/346724a0

Cited by 663 publications

(358 citation statements)

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“…Our results demonstrate that PPF is approximately linearly related to the [Cal,,,. This finding further supports the residual Ca hypothesis for PPF. Accumulated evidence from other groups suggests that the presynaptic site contributes to the maintenance of LTP in CA3-CA1 synapses (Bekkers and Stevens, 1990;Malinow and Tsien, 1990); however, our data show that neither an increase of the Ca transient nor a sustained increase of the [Cal,,, occurs Presynaptic Ca channels play a key role in synaptic transmission and different forms of synaptic plasticity. So far, most studies have been performed at the squid giant synapse (Llinas et al, 1976(Llinas et al, , 1981Augustine et al, 1985a,b) or the neuromuscular junction (Dodge and Rahamimoff, 1967;Katz and Miledi, 1968;Delaney et al, 1989).…”

contrasting

confidence: 50%

“…LTP is generally thought to be involved in learning and memory. Multiple lines of evidence including results of quanta1 analysis (Bekkers and Stevens, 1990;Malinow and Tsien, 1990;Kullmann and Nicoll, 1992;Liao et al, 1992;Malgaroli and Tsien, 1992) and the demonstration of postsynaptically released presumed retrograde messengers (Kom and Faber, 199 1;Fazeli, 1992) strongly suggest that the presynaptic site participates in the maintenance of LTP in area CA 1 of the hippocampus. Three mechanisms may underlie a presynaptic maintenance of LTP:…”

mentioning

confidence: 99%

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Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus

1994

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We examined the relationship between presynaptic calcium levels and postsynaptic potentials during normal synaptic transmission, paired- pulse facilitation (PPF), and long-term potentiation (LTP) in CA3-CA1 synapses of hippocampus. By selectively loading the presynaptic terminals with the calcium indicator fura-2, we simultaneously recorded a presynaptic calcium (Ca) transient and the corresponding field EPSP evoked by a single stimulus given to the Schaffer collateral- commissural pathway in guinea pig hippocampal slices. A volume average presynaptic Ca influx was obtained by taking the first time derivative of the Ca transient. Our data indicate that the synaptic transmission represented by the initial slope of the field EPSP is approximately proportional to the fourth power of the presynaptic Ca influx, the volume average Ca current. Our results in combination with similar findings at the squid giant synapse (Augustine et al., 1985b; Augustine and Charlton, 1986) suggest that the relationship between Ca influx and transmitter release is well conserved from the molluscan to the mammalian nervous system. A transient increase of the residual Ca level ([Ca]res) is generally thought to be the mechanism underlying PPF (Katz and Miledi, 1968; Charlton et al., 1982); however, the relationship between PPF and the presynaptic [Ca]res had not been examined before. Our results demonstrate that PPF is approximately linearly related to the [Ca]res. This finding further supports the residual Ca hypothesis for PPF. Accumulated evidence from other groups suggests that the presynaptic site contributes to the maintenance of LTP in CA3-CA1 synapses (Bekkers and Stevens, 1990; Malinow and Tsien, 1990); however, our data show that neither an increase of the Ca transient nor a sustained increase of the [Ca]res occurs in the presynaptic terminals during maintenance of LTP. This suggests that the presynaptic mechanism underlying LTP must be downstream to Ca influx.

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confidence: 99%

Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus

1994

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“…By analogy with studies of LTP in the CA1 region of the hippocampus, NO may act downstream of the NMDA receptor, diffusing to the presynaptic terminal to transmit information about postsynaptic activation. In LTP, this signal might result in increased neurotransmitter release (Bekkers and Stevens, 1990;Malinow and Tsien, 1990;Malgaroli et al, 1995), whereas in retinogeniculate development, this signal may result in regulation of presynaptic arbor size and position, because both NMDA receptor blockade (Hahm et al, 1991) and NOS blockade (in the present study) result in inappropriately placed retinogeniculate axon arbors. Determination of the extent of the similarity in the biochemical mechanisms underlying activity-dependent refinement of connections and LTP will require additional investigation.…”

Section: Discussionmentioning

confidence: 67%

“…In particular, LTP in the CA1 region of the hippocampus may share mechanisms in common with developmental remodeling (Goodman and Shatz, 1993). Postsynaptic activation of NMDA receptors is required to initiate LTP (Bliss and Collingridge, 1993), whereas maintenance of LTP may require presynaptic upregulation of neurotransmitter release (Bekkers and Stevens, 1990;Malinow and Tsien, 1990;Malgaroli et al, 1995). The development of sublaminae in the LGN represents an example of activity-dependent remodeling of connections that may show mechanistic similarities to LTP in the hippocampal CA1 region.…”

Section: Discussionmentioning

confidence: 99%

A Role for Nitric Oxide in the Development of the Ferret Retinogeniculate Projection

et al. 1996

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The ferret retinogeniculate projection segregates into eyespecific layers during the first postnatal week and into ON/OFF sublaminae, which receive inputs from either on-center or offcenter retinal ganglion cells, during the third and fourth postnatal weeks. The restriction of retinogeniculate axon arbors into eye-specific layers appears to depend on action potential activity (Shatz and Stryker, 1988) but does not require activation of NMDA receptors (Smetters et al., 1994). The formation of ON/OFF sublaminae is also activity-dependent and is disrupted by in vivo blockade of NMDA receptors (Hahm et al., 1991). To investigate a possible mechanism whereby blockade of postsynaptic NMDA receptors in the lateral geniculate nucleus (LGN) results in changes in the size and position of presynaptic axon arbors, we tested the role of the diffusible messenger nitric oxide (NO) in the development of the retinogeniculate pathway. We found previously that NO synthase (NOS) is transiently expressed in LGN cells during the refinement of retinogeniculate projections . In this study, treatment with N G -nitro-L-arginine (L-NoArg), an arginine analog that inhibits NOS, during the third and fourth postnatal weeks resulted in an overall pattern of sublamination that was significantly reduced compared with normal and control animals. Single retinogeniculate axon arbors were located in the middle of eye-specific layers rather than toward the inner or outer half as in normal or control animals. The effect of NOS inhibition was not a consequence of the hypertensive effect of L-NoArg. In contrast to the effect of L-NoArg on the formation of ON/OFF sublaminae, treatment with L-NoArg during the first postnatal week did not disrupt the formation of eye-specific layers. Biochemical assays indicated significant inhibition of NOS during both treatment periods. These data suggest that NO acts together with NMDA receptors in activity-dependent refinement of connections during a specific phase of retinogeniculate development. Key words: diffusible messenger; visual system; lateral geniculate nucleus (LGN); pattern formation; eye-specific layers; ON/ OFF sublaminae; neuronal activityThe precise pattern of connections underlying adult visual processing in mammals arises from the refinement of less specific connectivity present early in development. The mechanisms by which diffuse connections are refined rely at least in part on neuronal activity. In the ferret, retinogeniculate connections are refined in two distinct phases. During the first postnatal week, retinal axons within the lateral geniculate nucleus (LGN) segregate into eye-specific layers (Linden et al., 1981). During the third and fourth postnatal weeks, afferents to the A and A1 layers, which receive input from the contralateral and ipsilateral eye, respectively, further segregate into sublaminae. The inner sublamina receives inputs from on-center retinal ganglion cells, whereas the outer sublamina receives inputs from off-center retinal ganglion cells (Stryker and Zahs, 1983;Hahm and S...

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“…The possibility that p increases with LTP has been tested with some evidence supporting its involvement (1)(2)(3)(4) and other evidence weighing against it (5)(6)(7)(8)(9). One approach to addressing this question has been to test for associated changes in paired-pulse facilitation (PPF).…”

mentioning

confidence: 99%

Long-term potentiation involves increases in the probability of neurotransmitter release

Schulz

1997

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

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Biochemistry. In the article ''Identification by mass spectrometry of the phosphorylated residue responsible for activation of the catalytic domain of myosin I heavy chain kinase, a member of the PAK͞STE20 family'' by Joanna Szczepanowska, Xiaolong Zhang, Christopher J. Herring, Jun Qin, Edward D. Korn, and Hanna Brzeska, which appeared in number 16, August 5, 1997, of Proc. Natl. Acad. Sci. USA (94,(8503)(8504)(8505)(8506)(8507)(8508), the authors wish to note that in Fig. 3, the ions of m͞z 1345.3 and 1247.1 were incorrectly identified as b 13 and b 13 ⌬ , respectively, produced by cleavage of the peptide AS(Pi)VVGTTYW-MAPEVVK between E and V (Fig. 3 Inset). In fact, these ions are b 12 and b 12 ⌬ , produced by cleavage of the peptide between P and E. This correction has no effect on the conclusion that the phosphorylated residue is serine. Also, in Table 2, reference numbers 22-24 should be 21-23 (the reference in the legend is cited correctly) and the MIHCK sequence is from residue 624 to residue 638.Cell Biology. In the article ''Subtraction hybridization identifies a transformation progression-associated gene PEG-3 with sequence homology to a growth arrest and DNA damageinducible gene'' by Zao

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Presynaptic mechanism for long-term potentiation in the hippocampus

Abstract: Experiments analysing the statistical properties of synaptic transmission, before and after the induction of long-term potentiation (LTP), suggest that expression of LTP largely arises in a presynaptic mechanism--an increased probability of transmitter release.

Cited by 663 publications

References 29 publications

Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus

Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus

A Role for Nitric Oxide in the Development of the Ferret Retinogeniculate Projection

Long-term potentiation involves increases in the probability of neurotransmitter release

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