Specific long-lasting potentiation of synaptic transmission in hippocampal slices

Andersen, P.; Sundberg, S H; Sveen, O.; Wigström, Holger

doi:10.1038/266736a0

Cited by 455 publications

(155 citation statements)

References 4 publications

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“…This result should be expected from the previously shown input specificity of LLP (Andersen et al, 1977;McNaughton and Barnes, 1977). It also emphasizes the independence ofthe two inputs (see also Materials and Methods).…”

Section: As Shown Insupporting

confidence: 61%

Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents

Gustafsson¹,

Wigström²

1986

J. Neurosci.

156

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Cooperative effects between afferents on the induction of longlasting potentiation (LLP) of synaptic transmission were examined in the CA1 region of the hippocampal slice preparation. Synaptic activity was recorded extracellularly in the dendritic layer (stratum radiatum) as a field EPSP, and the amount of LLP produced was measured from the change in slope of the rising phase of this potential. Experiments were performed with the GABA antagonist picrotoxin in the bath solution in order to facilitate the induction of LLP. It is shown that under these conditions a test input evoked by single volleys (at 0.2 Hz) is potentiated when paired with brief tetani (2-15 impulses at 50 Hz) to a separate population of fibers in the stratum radiatum. For this potentiation to appear, the test input had to occur during the train or precede it by less than 40 msec. Maximal effects were observed with the test volley positioned in the early part of the tetanus, and were largely independent of train duration. The potentiation obtained in this manner reached a peak level after some 20 conjunction events, and its magnitude measured 10 min after conjunction was about half that which could be induced by homosynaptic tetanization. Prior homosynaptic potentiation occluded the potentiation induced by conjunction, suggesting an identity of their underlying mechanisms. A test input to the apical dendritic layer was potentiated also by inputs to the basal dendritic layer, although greater effects were observed with both inputs in the same dendritic layer. It is suggested that the conditioning effect is related to the postsynaptic depolarization created by the tetanus. The results support the recent proposal that LLP is induced by ionic flux through voltage-dependent synaptic channels.In the hippocampus, tetanic activation of afferents leads to a very prolonged increase in synaptic efficacy, known as longlasting potentiation (LLP) (Bliss and Gardner-Medwin, 1973;Bliss and Lomo, 1973;Douglas and Goddard, 1975;Lomo, 1966). Even though considerable work has been devoted to finding the mechanism(s) underlying LLP, this question is still unsettled, and there is even controversy whether the actual modification takes place on the pre-or postsynaptic side (e.g., see Dolphin et al., 1982;Douglas et al., 1982;Lynch et al., 1983; Skrede and Malthe-Sorenssen, 198 1; see also Bliss and Dolphin, 1982).Under normal conditions, LLP is induced by long stimulus trains giving rise to considerable activity in both presynaptic terminals and postsynaptic cells. It has recently been shown, however, that the induction of LLP is greatly facilitated when

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Section: As Shown Insupporting

confidence: 61%

Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents

Gustafsson¹,

Wigström²

1986

J. Neurosci.

156

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“…In young mice (2 mo), we confirmed the well-established input selectivity of LTP ( Fig. 2C) (Bliss and Lomo 1973;Andersen et al 1977). When four trains (1 sec, 100 Hz, 5 min apart) were applied 1 through S1, an LTP developed in the synapses tested via S1 (168 ‫ע‬ 10% of baseline 4 h after induction, n = 7, Fig.…”

supporting

confidence: 52%

Synapse specificity of long-term potentiation breaks down with aging

Ris¹,

Godaux²

2007

Learn. Mem.

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Memory shows age-related decline. According to the current prevailing theoretical model, encoding of memories relies on modifications in the strength of the synapses connecting the different cells within a neuronal network. The selective increases in synaptic weight are thought to be biologically implemented by long-term potentiation (LTP). Here, we report that tetanic stimulation of afferent fibers in slices from 12-mo-old mice triggers an LTP not restricted to the activated synapses. This phenomenon, which can be anticipated to hinder memory encoding, is suppressed by blocking either L-type Ca ++ channels or Ca ++ -induced Ca ++ release, both well known to become disregulated with aging.During the normal aging process, humans and animals experience age-related memory decline (Bach et al. 1999;Rosenzweig and Barnes 2003). Historically, it was thought that the primary contribution to the etiology of this decline was a massive loss of neurons in all the cortical layers and in the hippocampus (Brody 1955;Scheibel et al. 1976;Scheibel 1979). However, when it became possible to eliminate many of the confounding factors of the previous studies, this was proved to be a misconception (Burke and Barnes 2006). Nowadays, a great number of studies have identified multiple changes in Ca ++ -related electrophysiological processes as consistent biomarkers of aging (Landfield and Pitler 1984;Thibault and Landfield 1996;Norris et al. 1998;Thibault et al. 2001;Gant et al. 2006). One of the current prevailing hypotheses is that those Ca ++ dysregulations underlie many aspects of aging. However, the potential link between agerelated Ca ++ dysregulations and memory decline is still missing.For neurocomputing theorists, every memory is encoded in a neuronal network thanks to a change in the distribution of its synaptic weights (Zipser and Andersen 1988). Among the possible biological mechanisms, long-term potentiation (LTP) is the favored candidate to be at the basis of memory storage because this activity-induced increase in synaptic strength is (1) durable and (2) input-selective (restricted to the activated synapses). In the hippocampal synapses between Schaffer collaterals and CA1 pyramidal neurons, a single train of tetanic stimulation triggers a short-lasting LTP (S-LTP), which lasts 1-2 h, whereas multiple trains induce a long-lasting LTP (L-LTP) lasting >4 h (Huang and Kandel 1994;Abel et al. 1997). Potential age-related LTP defects have been sought out in the past. It has been reported that S-LTP in area CA1 from aged animals was normal when supra-threshold stimulation parameters were used (Moore et al. 1993;Burke and Barnes 2006) and showed deficits only when peri-threshold stimulation was applied (Barnes et al. 1992;Burke and Barnes 2006). The L-LTP triggered by multiple trains has been reported to be decreased in aged mice (18 mo) (Bach et al. 1999). In contrast, a brief 1-Hz paired-pulse stimulation has been found to induce an L-LTP in old mice but not in young animals (Huang and Kandel 2006). In our work, we focused on...

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“…First, LTP at certain synapses is associative, in that coactivation of weak inputs and strong inputs onto the same neuron can lead to strengthening of the weak inputs (McNaughton et al 1978;Levy and Steward 1979). Second, such LTP is synapse specific, in that synaptic strengthening occurs only at synapses of active, but not inactive, presynaptic afferents to the postsynaptic cell (Andersen et al 1977;Lynch et al 1977). LTP that exhibits these two properties -associativity and synapse specificity -is commonly referred to as associative or Hebbian LTP.…”

Section: Synaptic Mechanisms For Associative Learningmentioning

confidence: 99%

Synaptic Plasticity in the Lateral Amygdala: A Cellular Hypothesis of Fear Conditioning

Blair¹,

Schafe²,

Bauer³

et al. 2001

Learn. Mem.

548

360

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Fear conditioning is a form of associative learning in which subjects come to express defense responses to a neutral conditioned stimulus (CS) that is paired with an aversive unconditioned stimulus (US). Considerable evidence suggests that critical neural changes mediating the CS-US association occur in the lateral nucleus of the amygdala (LA). Further, recent studies show that associative long-term potentiation (LTP) occurs in pathways that transmit the CS to LA, and that drugs that interfere with this LTP also disrupt behavioral fear conditioning when infused into the LA, suggesting that associative LTP in LA might be a mechanism for storing memories of the CS-US association. Here, we develop a detailed cellular hypothesis to explain how neural responses to the CS and US in LA could induce LTP-like changes that store memories during fear conditioning. Specifically, we propose that the CS evokes EPSPs at sensory input synapses onto LA pyramidal neurons, and that the US strongly depolarizes these same LA neurons. This depolarization, in turn, causes calcium influx through NMDA receptors (NMDARs) and also causes the LA neuron to fire action potentials. The action potentials then back-propagate into the dendrites, where they collide with CS-evoked EPSPs, resulting in calcium entry through voltage-gated calcium channels (VGCCs). Although calcium entry through NMDARs is sufficient to induce synaptic changes that support short-term fear memory, calcium entry through both NMDARs and VGCCs is required to initiate the molecular processes that consolidate synaptic changes into a long-term memory.

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Specific long-lasting potentiation of synaptic transmission in hippocampal slices

Cited by 455 publications

References 4 publications

Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents

Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents

Synapse specificity of long-term potentiation breaks down with aging

Synaptic Plasticity in the Lateral Amygdala: A Cellular Hypothesis of Fear Conditioning

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