Presynaptically Expressed Long-Term Potentiation Increases Multivesicular Release at Parallel Fiber Synapses

Bender, Vanessa A.; Pugh, Jason R.; Jahr, Craig E.

doi:10.1523/jneurosci.2123-09.2009

Cited by 56 publications

(61 citation statements)

References 36 publications

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“…Our results extend previous findings made at cerebellar parallel fiber synapses (Bender et al 2009;Foster et al 2005) and hippocampal Schaffer collateral-CA1 terminals (Christie and Jahr 2006), which display low initial release probability but show MVR and postsynaptic receptor saturation following use-dependent increases in P. However, across different types of synapses, no defining principles have emerged that link the existence of MVR and saturation to other functional properties EPSCs are normalized to the baseline EPSC in the respective condition. D: summary data for AMPAR and NMDAR augmentation.…”

Section: Discussionsupporting

confidence: 87%

“…This suggests that the magnitude of similar forms of short-term enhancement at other synapses such as cerebellar parallel fibers (Beierlein et al 2007) or the calyx of held (Habets and Borst 2005) might also be strongly limited by postsynaptic saturation. In addition to expressing augmentation, CT synapses can undergo a presynaptic form of long-term potentiation (Castro-Alamancos and Calcagnotto 1999), and our data predict that saturation will become more prominent following long-term potentiation induction, similar to what has been observed at cerebellar parallel fibers (Bender et al 2009). …”

Section: Discussionsupporting

confidence: 80%

“…Increases in synaptic glutamate concentration associated with increases in release probability are most likely mediated by the simultaneous release of multiple vesicles from individual release sites (Bender et al 2009;Christie and Jahr 2006;Foster et al 2002). However, in principle such increases could also occur following the spillover and pooling of glutamate from closely spaced activated synapses (Carter and Regehr 2000;Marcaggi and Attwell 2005).…”

Section: Postsynaptic Saturation Of Ampars At Ct Synapsesmentioning

confidence: 99%

“…Both pre-and postsynaptic mechanisms underlie shortterm plasticity (Blitz et al 2004). Changes in the amount of transmitter released can be mediated by changes in release probability P. In turn, changes in P can be accompanied by changes in the number of simultaneously released vesicles at a given release site, resulting in changes in transmitter concentration in the synaptic cleft (Bender et al 2009;Foster et al 2005;Foster et al 2002;Higley et al 2009;Li et al 2009;Oertner et al 2002;Singer et al 2004;Wadiche and Jahr 2001). These forms of presynaptic plasticity can interact with the properties of postsynaptic receptors, such as receptor desensitization (Jones and Westbrook 1996;Trussell et al 1988) or saturation (Foster et al 2002;Harrison and Jahr 2003;Tong and Jahr 1994;Wadiche and Jahr 2001).…”

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confidence: 99%

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Receptor saturation controls short-term synaptic plasticity at corticothalamic synapses

Sun¹,

Beierlein²

2011

Journal of Neurophysiology

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Sun Y-G, Beierlein M. Receptor saturation controls short-term synaptic plasticity at corticothalamic synapses. J Neurophysiol 105: 2319 -2329, 2011. First published February 16, 2011 doi:10.1152/jn.00942.2010.-Glutamatergic synapses of layer 6 corticothalamic (CT) neurons form a major excitatory input onto thalamic relay cells, allowing neocortex to continuously control sensory information processing in thalamic circuits. CT synapses display both short-and long-term forms of use-dependent synaptic enhancement, mediated at least in part by increases in the probability of transmitter release. At some synapses, such increases in release probability are accompanied by a higher degree of multivesicular release (MVR) and larger glutamate transients at individual release sites, resulting in the saturation of postsynaptic receptors. The extent to which MVR and postsynaptic saturation interact and control shortterm plasticity at CT synapses is not known. Here we examined two distinct presynaptic forms of short-term enhancement, facilitation and augmentation, at CT synapses contacting relay neurons in the ventrobasal nucleus of the mouse thalamus. We found that, in the presence of the low-affinity antagonist ␥-D-glutamylglycine, to relieve postsynaptic DL-␣-amino-3-hydroxy-5-methylisox azole-propionic acid (AMPA) receptor saturation, the magnitude of facilitation and augmentation increased. Whereas receptor saturation was prominent for both AMPA and N-methyl-D-aspartate receptors, desensitization of AMPA receptors did not significantly alter short-term plasticity. Our results suggest that at CT synapses the activity-dependent increase in synaptic strength is controlled by postsynaptic receptor saturation.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionsupporting

confidence: 80%

Section: Postsynaptic Saturation Of Ampars At Ct Synapsesmentioning

confidence: 99%

mentioning

confidence: 99%

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Receptor saturation controls short-term synaptic plasticity at corticothalamic synapses

Sun¹,

Beierlein²

2011

Journal of Neurophysiology

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“…In the cerebellum, repetitive parallel fiber (PF) stimulation triggers presynaptic LTP at PF to Purkinje cell synapses. Induction does not require postsynaptic glutamate receptor activation or Ca 2þ rises but, as for MF-LTP, requires cAMP/PKA signaling (Sakurai 1987;Shibuki and Okada 1992;Salin et al 1996b;Storm et al 1998;Linden and Ahn 1999;Bender et al 2009). Similar presynaptic LTP was subsequently observed at PF to molecular layer interneuron synapses (Rancillac and Crepel 2004;Bender et al 2009).…”

Section: Mossy Fiber To Ca3 Pyramidal Cell Synapse As a Model For Prementioning

confidence: 99%

Presynaptic LTP and LTD of Excitatory and Inhibitory Synapses

Castillo

2011

Cold Spring Harbor Perspectives in Biology

145

134

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Ubiquitous forms of long-term potentiation (LTP) and depression (LTD) are caused by enduring increases or decreases in neurotransmitter release. Such forms or presynaptic plasticity are equally observed at excitatory and inhibitory synapses and the list of locations expressing presynaptic LTP and LTD continues to grow. In addition to the mechanistically distinct forms of postsynaptic plasticity, presynaptic plasticity offers a powerful means to modify neural circuits. A wide range of induction mechanisms has been identified, some of which occur entirely in the presynaptic terminal, whereas others require retrograde signaling from the postsynaptic to presynaptic terminals. In spite of this diversity of induction mechanisms, some common induction rules can be identified across synapses. Although the precise molecular mechanism underlying long-term changes in transmitter release in most cases remains unclear, increasing evidence indicates that presynaptic LTP and LTD can occur in vivo and likely mediate some forms of learning.A t several excitatory and inhibitory synapses, neuronal activity can trigger enduring increases or decreases in neurotransmitter release, thereby producing long-term potentiation (LTP) or long-term depression (LTD) of synaptic strength, respectively. In the last decade, many studies have revealed that these forms of plasticity are ubiquitously expressed in the mammalian brain, and accumulating evidence indicates that they may underlie behavioral adaptations occurring in vivo. These studies have also uncovered a wide range of induction mechanisms, which converge on the presynaptic terminal where an enduring modification in the neurotransmitter release process takes place. Interestingly, presynaptic forms of LTP/ LTD can coexist with classical forms of postsynaptic plasticity. Such diversity expands the dynamic range and repertoire by which neurons modify their synaptic connections. This review discusses mechanistic aspects of presynaptic LTP and LTD at both excitatory and inhibitory synapses in the mammalian brain, with an emphasis on recent findings. INDUCTION MECHANISMSAs illustrated in Figure 1, presynaptic LTP/LTD at both excitatory and inhibitory synapses can be induced in a homosynaptic or heterosynaptic manner, with induction occurring either entirely at the presynaptic terminal or requiring a retrograde messenger arising from the postsynaptic neuron. Each of these four induction

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Dynamics of nascent and active zone ultrastructure as synapses enlarge during long‐term potentiation in mature hippocampus

Bell¹,

Bourne²,

Chirillo³

et al. 2014

J of Comparative Neurology

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Nascent zones and active zones are adjacent synaptic regions that share a postsynaptic density, but nascent zones lack the presynaptic vesicles found at active zones. Here dendritic spine synapses were reconstructed through serial section electron microscopy (3DEM) and EM tomography to investigate nascent zone dynamics during long-term potentiation (LTP) in mature rat hippocampus. LTP was induced with theta-burst stimulation and comparisons were made to control stimulation in the same hippocampal slices at 5 minutes, 30 minutes, and 2 hours post-induction and to perfusion-fixed hippocampus in vivo. Nascent zones were present at the edges of ~35% of synapses in perfusion-fixed hippocampus and as many as ~50% of synapses in some hippocampal slice conditions. By 5 minutes, small dense core vesicles known to transport active zone proteins moved into more presynaptic boutons. By 30 minutes, nascent zone area decreased without significant change in synapse area, suggesting that presynaptic vesicles were recruited to pre-existing nascent zones. By 2 hours, both nascent and active zones were enlarged. Immunogold labeling revealed that glutamate receptors can be found in nascent zones; however, average distances from nascent zones to docked presynaptic vesicles ranged from 170±5 nm in perfusion-fixed hippocampus to 251±4 nm at enlarged synapses by 2 hours during LTP. Prior stochastic modeling suggests that falloff in glutamate concentration reduces the probability of glutamate receptor activation from 0.4 at the center of release to 0.1 just 200 nm away. Thus, conversion of nascent zones to functional active zones likely requires the recruitment of presynaptic vesicles during LTP.

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Presynaptically Expressed Long-Term Potentiation Increases Multivesicular Release at Parallel Fiber Synapses

Cited by 56 publications

References 36 publications

Receptor saturation controls short-term synaptic plasticity at corticothalamic synapses

Receptor saturation controls short-term synaptic plasticity at corticothalamic synapses

Presynaptic LTP and LTD of Excitatory and Inhibitory Synapses

Dynamics of nascent and active zone ultrastructure as synapses enlarge during long‐term potentiation in mature hippocampus

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