Learning‐related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long‐term potentiation

Otto, Tim; Eichenbaum, Howard; Wiener, Sidney I.; Wible, Cynthia G.

doi:10.1002/hipo.450010206

Cited by 282 publications

(178 citation statements)

References 47 publications

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“…These complex spikes mimic the firing pattern of CA1 neurons in vivo (Kandel and Spencer, 1961;Suzuki and Smith, 1985;Thomas et al, 1998). Moreover, burst firing in CA1 occurs at theta frequencies (5-12 Hz) during exploratory behavior (Otto et al, 1991) and is required for 5 Hz LTP induction in vitro (Thomas et Figure 6. The deficit in 5 Hz LTP in AI rats is not linked to a loss of NMDA receptor function.…”

Section: Discussionmentioning

confidence: 80%

Theta-Frequency Synaptic Potentiation in CA1In VitroDistinguishes Cognitively Impaired from Unimpaired Aged Fischer 344 Rats

et al. 2002

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Hippocampal-dependent learning and memory deficits have been well documented in aging rodents. The results of several recent studies have suggested that these deficits arise from weakened synaptic plasticity within the hippocampus. In the present study, we examined the relationship between hippocampal long-term potentiation (LTP) in vitro and spatial learning in aged (24-26 months) Fischer 344 rats. We found that LTP induced in the CA1 region using theta-frequency stimulation (5 Hz) is selectively impaired in slices from a subpopulation of aged rats that had shown poor spatial learning in the Morris water maze. LTP at 5 Hz in aged rats that did not show learning deficits was similar to that seen in young (4-6 months) controls. We also found that 5 Hz LTP amplitude strongly correlated with individual learning performance among aged rats. The difference in 5 Hz LTP magnitude among aged rats was not attributable to an altered response to 5 Hz stimulation or to differences in the NMDA receptormediated field EPSP. In addition, no performance-related differences in LTP were seen when LTP was induced with 30 or 70 Hz stimulation protocols. Finally, both 5 Hz LTP and spatial learning in learning-impaired rats were enhanced with the selective muscarinic M 2 antagonist ]benzodiazepin-6-one). These findings reinforce the idea that distinct types of hippocampal LTP offer mechanistic insight into age-associated cognitive decline.

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Section: Discussionmentioning

confidence: 80%

Theta-Frequency Synaptic Potentiation in CA1In VitroDistinguishes Cognitively Impaired from Unimpaired Aged Fischer 344 Rats

et al. 2002

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“…We have shown previously that NMDARdependent LTP can be induced by pairing theta-burst stimulation (TBS) of presynaptic inputs with a modest postsynaptic depolarization, so that the excitatory postsynaptic potentials (EPSPs) during the burst are suprathreshold (5). This theta-burst pairing (TBP) is Hebbian in the sense that presynaptic bursts are temporally correlated with postsynaptic spikes, and this activity pattern is thought to mimic the firing patterns seen in hippocampus during behavioral learning in vivo (13). After TBP, there was an immediate increase in EPSPs followed by a gradual increase that developed over 15-30 min ( Fig.…”

Section: Resultsmentioning

confidence: 97%

Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation

Yang

Wang

Frerking

et al. 2008

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

132

126

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Trafficking of AMPA subtype glutamate receptors (AMPARs) from intracellular compartments to synapses is thought to be a major mechanism underlying the expression of long-term potentiation (LTP), a cellular substrate for learning and memory. However, it remains unclear whether the AMPAR trafficking that takes place during LTP is due to a targeted insertion of AMPARs directly into the synapse or delivery to extrasynaptic sites followed by translocation into the synapse. Here, we provide direct physiological evidence that LTP induced by a theta-burst pairing and tetanic stimulation protocols causes the rapid delivery of AMPARs to a perisynaptic site. Perisynaptic AMPARs do not normally detect synaptically released glutamate but can do so when the glial glutamate transporter EAAT1 is inhibited. AMPARs can be detected at this perisynaptic site before, but not after, the full expression of LTP. The appearance of perisynaptic AMPARs requires postsynaptic exocytosis, PKA signaling, and the C-terminal region of GluR1 subunit of AMPARs but not actin polymerization. Actin polymerization after LTP induction is required to retain AMPARs at the perisynaptic site after their appearance. Low-frequency stimulation given shortly after LTP induction leads to activity-dependent removal of perisynaptic AMPARs and suppresses the subsequent expression of LTP. These results demonstrate that AMPARs are rapidly trafficked to perisynaptic sites shortly after LTP induction and suggest that the delivery and maintenance of perisynaptic AMPARs may serve as a checkpoint in the expression of LTP.actin ͉ dendritic spine ͉ trafficking ͉ TBOA ͉ two-photon imaging A ctivity-induced modification of neuronal connections is essential for the development of the nervous system and may underlie some forms of learning and memory. One widely examined form of synaptic plasticity is long-term potentiation (LTP). LTP leads to the synaptic insertion of glutamate receptors of the AMPA subtype (AMPARs) (1-4). Recent studies also suggest that this synaptic incorporation of AMPARs may stabilize spine modifications associated with LTP (5, 6). Postsynaptic exocytosis (7,8), PKA activity (9), and AMPARs containing the GluR1 subunit (10) are implicated in the synaptic incorporation of AMPARs during LTP, but it remains unclear whether LTP leads to the direct insertion of AMPARs at the postsynaptic density (PSD) or to insertion at extrasynaptic regions followed by translocation into the PSD.Consistent with the latter idea, AMPAR targeting from intracellular compartments to the cell surface can occur via mechanisms that are distinct from AMPAR targeting from the cell surface to the synapse (11). By visualizing the movement of transfected AMPAR subunits or specific domains of AMPAR subunits in culture, trafficking of AMPARs can be observed in response to LTP induced by synaptic activity or chemical induction protocols. Using this approach, studies have found that AMPARs containing GluR1 can be inserted into the plasma membrane from intracellular stores (2). Lateral mobili...

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“…First, LTP requires a short timescale associated with bursts of action potentials separated by ϳ10 ms (Pike et al, 1999;Watanabe et al, 2002), a condition likely to depolarize CA1 dendrites strongly (Buzsaki, 2002;Lisman and Spruston, 2005). LTP also requires a longer timescale over which activity occurs repeatedly at 200 ms intervals, the approximate period of the theta rhythm (Larson and Lynch, 1986;Rose and Dunwiddie, 1986;Otto et al, 1991). These requirements for potentiation have not been observed in neocortical synapses (Sjöström et al, 2001;Froemke and Dan, 2002) or in hippocampal cultures (Wang et al, 2005), indicating that some biophysical requirements for inducing bidirectional synaptic plasticity are specific to CA1 pyramidal neurons.…”

Section: Conditions For a Bidirectional Learning Rulementioning

confidence: 99%

Malleability of Spike-Timing-Dependent Plasticity at the CA3-CA1 Synapse

Wittenberg

Wang

2006

Journal of Neuroscience

297

416

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The magnitude and direction of synaptic plasticity can be determined by the precise timing of presynaptic and postsynaptic action potentials on a millisecond timescale. In vivo, however, neural activity has structure on longer timescales. Here we show that plasticity at the CA3-CA1 synapse depends strongly on parameters other than millisecond spike timing. As a result, the notion that a single spiketiming-dependent plasticity (STDP) rule alone can fully describe the mapping between neural activity and synapse strength is invalid. We have begun to explore the influence of additional behaviorally relevant activity parameters on STDP and found conditions under which underlying spike-timing-dependent rules for potentiation and depression can be separated from one another. Potentiation requires postsynaptic burst firing at 5 Hz or higher, a firing pattern that occurs during the theta rhythm. Potentiation is measurable after only tens of presynaptic-before-postsynaptic pairings. Depression requires hundreds of pairings but has less stringent long timescale requirements and broad timing dependence. By varying these parameters, we obtain STDP curves that are long-term potentiation only, bidirectional, or long-term depression only. This expanded description of the CA3-CA1 learning rule reconciles apparent contradictions between spike-timing-dependent plasticity and previous work at CA3-CA1 synapses.

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Learning‐related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long‐term potentiation

Cited by 282 publications

References 47 publications

Theta-Frequency Synaptic Potentiation in CA1In VitroDistinguishes Cognitively Impaired from Unimpaired Aged Fischer 344 Rats

Theta-Frequency Synaptic Potentiation in CA1In VitroDistinguishes Cognitively Impaired from Unimpaired Aged Fischer 344 Rats

Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation

Malleability of Spike-Timing-Dependent Plasticity at the CA3-CA1 Synapse

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