Long-term potentiation and evidence for novel synaptic association in CA1 stratum oriens of rat hippocampus.

Otani, Satoru; Connor, J. A.; Levy, William B.

doi:10.1101/lm.2.2.101

Cited by 14 publications

(11 citation statements)

References 25 publications

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“…In particular, there appear to be functionally separate dendritic compartments corresponding to the anatomical domains we used for inducing LTP and LTD. Our findings further highlight the integrative capability of CA1 neurons of the mouse hippocampus, particularly, in regard to the induction and expression of opposing forms of synaptic plasticity within the same cell [12], [25], [38], [39], [40], [41], [42], [43]. Our main findings are summarized as follows: 1) that intracompartmental interactions are stronger in magnitude than transcompartmental ones, 2) that the magnitude of the interaction depends on the time separation between LTP and LTD inductions, 3) that during intracompartmental interference between LTP and LTD, only the subsequent form of synaptic plasticity is affected, 4) that cooperation and interference between LTP and LTD can not occur at the same time intervals, and 5) that the intracompartmental interference between LTP and LTD depends on new protein synthesis.…”

Section: Discussionsupporting

confidence: 53%

Interaction between Long-Term Potentiation and Depression in CA1 Synapses: Temporal Constrains, Functional Compartmentalization and Protein Synthesis

Pavlowsky

Alarcón

2012

PLoS ONE

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Information arriving at a neuron via anatomically defined pathways undergoes spatial and temporal encoding. A proposed mechanism by which temporally and spatially segregated information is encoded at the cellular level is based on the interactive properties of synapses located within and across functional dendritic compartments. We examined cooperative and interfering interactions between long-term synaptic potentiation (LTP) and depression (LTD), two forms of synaptic plasticity thought to be key in the encoding of information in the brain. Two approaches were used in CA1 pyramidal neurons of the mouse hippocampus: (1) induction of LTP and LTD in two separate synaptic pathways within the same apical dendritic compartment and across the basal and apical dendritic compartments; (2) induction of LTP and LTD separated by various time intervals (0–90 min). Expression of LTP/LTD interactions was spatially and temporally regulated. While they were largely restricted within the same dendritic compartment (compartmentalized), the nature of the interaction (cooperation or interference) depended on the time interval between inductions. New protein synthesis was found to regulate the expression of the LTP/LTD interference. We speculate that mechanisms for compartmentalization and protein synthesis confer the spatial and temporal modulation by which neurons encode multiplex information in plastic synapses.

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Section: Discussionsupporting

confidence: 53%

Interaction between Long-Term Potentiation and Depression in CA1 Synapses: Temporal Constrains, Functional Compartmentalization and Protein Synthesis

Pavlowsky

Alarcón

2012

PLoS ONE

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“…jneurosci.org as supplemental material). However, we cannot rule out the existence of heterosynaptic forms of synaptic plasticity in basal dendrites that may account for this effect (Otani et al, 1995). Despite this limitation, we did observe capture of L-LTP within the basilar compartment ( Fig.…”

Section: Synaptic Capture Of L-ltp Is Similar In Apical and Basal Denmentioning

confidence: 68%

“…Here we extended previous studies on synaptic capture in two ways: (1) we investigated the interaction between two inputs within the stratum oriens, and (2) we explored the interaction across the apical and basilar dendritic compartments of CA1 neurons. We found that, despite the differences in the mechanisms for induction and expression of LTP in basal and apical dendrites (Arai et al, 1994;Leung and Shen, 1995;Otani et al, 1995;Haley et al, 1996;Son et al, 1996;Cavus and Teyler, 1998;Kloosterman et al, 2001;Kawakami et al, 2003;Kramar and Lynch, 2003), E-LTP, L-LTP, and intracompartmental capture of L-LTP in each dendritic compartment could be induced with the same kind of stimulation protocols. In addition, we observed that the capture of L-LTP across dendritic compartments required a stronger marking stimulation than that required for the capture of L-LTP within the same compartment.…”

Section: Discussionmentioning

confidence: 84%

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Capture of the Late Phase of Long-Term Potentiation within and across the Apical and Basilar Dendritic Compartments of CA1 Pyramidal Neurons: Synaptic Tagging Is Compartment Restricted

Alarcón

Barco²,

Kandel³

2006

J. Neurosci.

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Studies in the rodent hippocampus have demonstrated that when the late phase of long-term potentiation (L-LTP) is induced in a set of synapses by suprathreshold stimulation, L-LTP can also be expressed by other synapses receiving subthreshold stimulation, a phenomenon usually referred as "capture of L-LTP." Because the pyramidal neurons in the mammalian hippocampus have both apical and basal dendrites, we have now investigated whether capture of L-LTP, previously described only within the apical dendritic compartment, can also take place within the basilar dendritic compartment and, if so, whether capture can be accomplished from one dendritic compartment to the other. We found that capture of L-LTP can also occur within the basilar dendritic compartment and that the tagging signal that enables capture appears to be the same in both dendritic compartments. However, capture across compartments, between the apical and basilar dendrites, follows different rules and requires a stronger triggering stimulation than capture within a compartment. These results suggest that the tag appears specific to a compartment either apical or basilar and that an additional mechanism may be required to capture across compartments.

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“…On the other hand, the spread of synaptic modification can also be mediated by signalling within the neuron. On the postsynaptic side, LTP at one synaptic input can result in heterosynaptic modification of other convergent inputs [14][15][16][17][18][19] . On the presynaptic side, changes may spread through the cytoplasm to other divergent outputs.…”

mentioning

confidence: 99%

Propagation of activity-dependent synaptic depression in simple neural networks

Fitzsimonds

Song

Poo

1997

Nature

166

125

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Triple whole-cell recordings from simple networks of cultured hippocampal neurons show that induction of long-term depression at glutamatergic synapses is accompanied by a back propagation of depression to input synapses on the dendrite of the presynaptic neuron. The depression also propagates laterally to divergent outputs of the presynaptic neuron and to convergent inputs on the postsynaptic neuron. There is no forward propagation of depression to the output of the postsynaptic neuron and no presynaptic propagation accompanying long-term depression at GABAergic synapses. Activity-induced synaptic modification is therefore not restricted to the activated synapse, but selectively propagates throughout the neural network.The development and plasticity of the nervous system involve activity-dependent modification of synaptic connections 1-3 . Longterm potentiation (LTP) and long-term depression (LTD) of central synapses induced by repetitive activity in various regions of the brain have been implicated as the cellular mechanisms that underlie learning and memory [4][5][6][7] . These modifications are known to be input-specific, so only activated pathways are affected. But within the vicinity of activated pathways, other non-activated synapses also become modified, leading to more distributed synaptic modifications within a neural network. For example, LTP generated at one synaptic input to a CA1 hippocampal neuron was found to spread to adjacent synapses on the same or on a different postsynaptic neuron [8][9][10][11] and to result in LTD in more distant neurons 12,13 . Such spread of synaptic modification appears to depend on membranepermeable or secreted factors released by the activated synapse, and the extent of influence on other synapses depends on their physical proximity. On the other hand, the spread of synaptic modification can also be mediated by signalling within the neuron. On the postsynaptic side, LTP at one synaptic input can result in heterosynaptic modification of other convergent inputs [14][15][16][17][18][19] . On the presynaptic side, changes may spread through the cytoplasm to other divergent outputs. In Xenopus nerve-muscle cultures, LTD induced at one neuromuscular synapse can propagate to other synapses made by the same neuron onto other myocytes, apparently by signalling within the neuronal cytoplasm 20 . A similar presynaptic cytoplasmic mechanism may also account for the spread of shortterm depression of inhibitory synapses observed in cerebellar slices 21 .Here we find that induction of LTD at glutamatergic synapses within small networks of cultured hippocampal neurons is accompanied by a retrograde spread of depression to synapses on the dendrites of the presynaptic neurons (back propagation). The depression also spreads laterally to synapses made by divergent outputs of the presynaptic neuron (presynaptic lateral propagation) or to convergent inputs on the postsynaptic neurons (postsynaptic lateral propagation). In contrast, there was no forward propagation of depression to output s...

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Long-term potentiation and evidence for novel synaptic association in CA1 stratum oriens of rat hippocampus.

Cited by 14 publications

References 25 publications

Interaction between Long-Term Potentiation and Depression in CA1 Synapses: Temporal Constrains, Functional Compartmentalization and Protein Synthesis

Interaction between Long-Term Potentiation and Depression in CA1 Synapses: Temporal Constrains, Functional Compartmentalization and Protein Synthesis

Capture of the Late Phase of Long-Term Potentiation within and across the Apical and Basilar Dendritic Compartments of CA1 Pyramidal Neurons: Synaptic Tagging Is Compartment Restricted

Propagation of activity-dependent synaptic depression in simple neural networks

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