Theta burst stimulation is optimal for induction of LTP at both apical and basal dendritic synapses on hippocampal CA1 neurons (original) (raw)
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Hippocampus, 2016
The hippocampal synapses display a conspicuous ability for long-term plasticity, which is thought to contribute to learning and memory. Previous research has shown that long-term potentiation (LTP) greatly differs between the dorsal (DH) and ventral (VH) CA1 hippocampal synapses when induced by high-frequency stimulation. In this study, using rat hippocampal slices and more physiologically relevant activity patterns based on the frequency of the theta rhythm (i.e. theta-burst stimulation, TBS) we found that the DH compared with the VH displayed a higher ability for induction and stability of NMDA receptor-dependent LTP of the field excitatory postsynaptic potential. Nevertheless, the maximal magnitude of LTP was similar in the two hippocampal segments. Blockade of GABA B receptors prevented the LTP induction by the minimal effective TBS and reduced the magnitude of LTP induced by longer TBS. TBS produced a threefold higher facilitation of the synaptic burst responses in the DH compared with the VH, accompanied by a strong enhancement in the postsynaptic excitation in the DH but mostly depression in the VH. The DH displayed NMDA receptordependent and NMDA receptor-independent facilitation, but the facilitation in the VH was only NMDA receptor-dependent. Also, the TBS-associated activity of GABA B receptors was higher in the DH than in the VH. The different response profiles during TBS could underlie the differences in LTP between the two hippocampal segments. L-type voltage-dependent calcium channels (L-VDCC) and the metabotropic glutamate receptor-5 (mGluR5) equally contributed in DH and VH to compound LTP induced by relatively long TBS. We propose that these dorsoventral differences in synaptic plasticity reflect specializations of the intrinsic circuitry of the hippocampus, that are involved in the distinct information processing performed by the two hippocampal segments and could effectively support the contribution
Brain Research, 1989
Induction of long-term potentiation (LTP) by asynchronous stimulation of converging afferents was studied in hippocampal slices. Three stimulation electrodes were positioned to activate separate groups of Schaffer-commissural inputs to a population of CA1 pyramidal cells. Patterned stimulation consisted of a single coincident priming pulse to all 3 electrodes followed by a burst of 4 pulses (100 Hz) to the first input (S1) at a delay of 180 ms, to the second ($2) at a delay of 200 ms, and to the third ($3) at a delay of 220 ms. This pattern was repeated 10 times at 5-s intervals. The magnitude of LTP induced (measured 20 min after stimulation) was greatest for the first stimulated input, intermediate for the second, and least for the third. Intracellular recordings indicated that the greatest postsynaptic depolarization occurred during the period of $2 stimulation; thus the magnitude of LTP induced was not simply dependent on the degree of depolarization during afferent activation. Rather, sustained depolarization after synaptic activation could contribute to LTP induction by prolonging the activity of N-methyI-D-aspartate receptor-gated channels. Earlier-arriving bursts may also trigger an inhibitory process that reduces the effectiveness of later bursts for inducing LTP.
Learning & Memory, 2016
The ability of the ventral hippocampus (VH) for long-lasting long-term potentiation (LTP) and the mechanisms underlying its lower ability for short-lasting LTP compared with the dorsal hippocampus (DH) are unknown. Using recordings of field excitatory postsynaptic potentials (EPSPs) from the CA1 field of adult rat hippocampal slices, we found that 200-Hz stimulation induced nondecremental LTP that was maintained for at least 7 h and was greater in the DH than in the VH. The interaction of NMDA receptors with L-type voltage-dependent calcium channels appeared to be more effective in the DH than in the VH. Furthermore, the LTP was significantly enhanced in the DH only, between 2 and 5 h post-tetanus. Furthermore, the mGluR5 contributed to the post-tetanic potentiation more in the VH than in the DH.
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1998
Long-term potentiation (LTP), a persistent enhancement of synaptic transmission that may be involved in some forms of learning and memory, is induced at excitatory synapses in the CA1 region of the hippocampus by coincident presynaptic and postsynaptic activity. Although action potentials back-propagating into dendrites of hippocampal pyramidal cells provide sufficient postsynaptic activity to induce LTP under some in vitro conditions, it is not known whether LTP can be induced by patterns of postsynaptic action potential firing that occur in these cells in vivo. Here we report that a characteristic in vivo pattern of action potential generation in CA1 pyramidal cells known as the complex spike burst enables the induction of LTP during theta frequency synaptic stimulation in the CA1 region of hippocampal slices maintained in vitro. Our results suggest that complex spike bursting may have an important role in synaptic processes involved in learning and memory formation, perhaps by pr...
The Journal of Physiology, 2013
• N -Methyl-D-aspartate receptor (NMDAR)-dependent potentiation of synaptic transmission is widely accepted as a cellular model of learning and memory. • It is most often studied in the CA1 area of rat hippocampal slices where it comprises a decremental and a sustained phase, which are commonly referred to as short-term potentiation (STP) and long-term potentiation (LTP), respectively. • In this study we show for the first time that STP and LTP are triggered by the activation of different classes of NMDARs and that STP itself comprises two pharmacologically and kinetically distinct components. • We suggest that the mechanistic separation of STP and LTP is likely to have important functional implications in that these two forms of synaptic plasticity can subserve unique physiological functions in a behaving animal.
Neuroscience Letters, 1999
Long-term potentiation (LTP) is a popular model for the synaptic changes that may occur during learning and memory; it involves a strengthening of synaptic response and is readily induced in the hippocampus, an area of the brain implicated in learning and memory. Previous research on LTP has focused on`early' components of the hippocampal circuitry, that is, the dentate gyrus and areas CA1 and CA3. This paper examines the plasticity of the CA1-subiculum pathway; we extend our previous work in this area demonstrating that the projection from area CA1 to subiculum sustains theta-patterned stimulus-induced LTP in vivo. We show that this pathway remains potentiated over a long period (3 h). Furthermore, once this projection is potentiated, it seems resistant to further episodes of high-frequency stimulation. We discuss the implications of these ®ndings for theories of hippocampal-cortical interaction during the biological consolidation of memory. q
Hippocampus, 2012
Hippocampal synaptic plasticity in the form of long-term potentiation (LTP) and long-term depression (LTD) is likely to enable synaptic information storage in support of memory formation. The mouse brain has been subjected to intensive scrutiny in this regard; however, a multitude of studies has examined synaptic plasticity in the hippocampal slice preparation, whereas very few have addressed synaptic plasticity in the freely behaving mouse. Almost nothing is known about the frequency or N-methyl-D-aspartate receptor (NMDAR) dependency of hippocampal synaptic plasticity in the intact mouse brain. Therefore, in this study, we investigated the forms of synaptic plasticity that are elicited at different afferent stimulation frequencies. We also addressed the NMDAR dependency of this phenomenon. Adult male C57BL/6 mice were chronically implanted with a stimulating electrode into the Schaffer collaterals and a recording electrode into the Stratum radiatum of the CA1 region. To examine synaptic plasticity, we chose protocols that were previously shown to produce either LTP or LTD in the hippocampal slice preparation. Low-frequency stimulation (LFS) at 1 Hz (900 pulses) had no effect on evoked responses. LFS at 3 Hz (ranging from 200 up to 2 3 900 pulses) elicited short-term depression (STD, <45 min). LFS at 3 Hz (1,200 pulses) elicited slow-onset potentiation, high-frequency stimulation (HFS) at 100 Hz (100 or 200 pulses) or at 50 Hz was ineffective, whereas 100 Hz (50 pulses) elicited short-term potentiation (STP). HFS at 100 Hz given as 2 3 30, 2 3 50, or 4 3 50 pulses elicited LTP (>24 h). Theta-burst stimulation was ineffective. Antagonism of the NMDAR prevented STD, STP, and LTP. This study shows for the first time that protocols that effectively elicit persistent synaptic plasticity in the slice preparation elicit distinctly different effects in the intact mouse brain. Persistent LTD could not be elicited with any of the protocols tested. Plasticity responses are NMDAR dependent, suggesting that these phenomena are relevant for hippocampus-dependent learning. V V C 2012 Wiley Periodicals, Inc.
Journal of Neuroscience, 2009
Although plasticity at excitatory synapses is widely studied as a mechanism for memory formation, less is known about the properties and mechanisms underlying activity-dependent changes in excitability. Using extracellular and intracellular recordings in hippocampal slices, we find that short trains (2-3 s) of Schaffer collateral fiber stimulation delivered at 5 Hz induce a robust and persistent increase in the excitability of CA1 pyramidal cells in the absence of synaptic potentiation. This change in excitability is input specific, NMDA receptor dependent, and is not accompanied by lasting changes in either inhibitory synaptic transmission or somatic excitability. Although many of these properties are similar to those seen in synaptic long-term potentiation (LTP), the increase in CA1 pyramidal cell excitability was not blocked by inhibitors of several protein kinases required for the induction of LTP by theta frequency stimulation. Instead, 5 Hz stimulation-induced changes in neuronal excitability were blocked by inhibitors of the protein phosphatase calcineurin. Together, our results suggest that very brief bouts of theta frequency synaptic activity induce a selective, persistent, and dendritically localized increase in CA1 pyramidal cell excitability that might have an important role in both information storage and metaplasticity.
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2003
Experimental evidence suggests that the hippocampal theta rhythm plays a critical role in learning. Previous studies have shown long-term potentiation (LTP) to be preferentially induced with stimulation on the peak of local theta rhythm in region CA1 in anesthetized rats and with stimulation of the perforant path at the peak of theta in both anesthetized and behaving animals. We set out to determine the effects of tetanic burst stimulation in stratum radiatum of region CA1 in awake behaving animals, delivered during either the peak or the trough of the theta rhythm in the EEG. Bursts delivered to the peak resulted in an increase of 17.9 +/- 0.94% in potential slope. When identical stimulation bursts were delivered to the trough of local theta waves, the potential slope decreased 12.9 +/- 1.03%. This is the first report of LTP being preferentially induced at the peak of local theta rhythm in behaving animals in region CA1 and that LTD was found in response to tetanic stimulation at t...