Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition

Wigström, Holger; Gustafsson, Bengt

doi:10.1038/301603a0

Cited by 330 publications

(173 citation statements)

References 21 publications

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“…If inhibi-tion were left intact, high-frequency stimulation would produce a larger NMDA current in the presence of DA caused by the inhibition of GABA release, thereby facilitating synaptic plasticity. Indeed, in agreement with studies in the hippocampus (Wigstrom and Gustafsson, 1983), inhibiting GABA release in the NAc facilitates LTP (Pennartz et al, 1993).…”

Section: Discussionsupporting

confidence: 71%

Dopamine Excites Nucleus Accumbens Neurons through the Differential Modulation of Glutamate and GABA Release

Hjelmstad¹

2004

J. Neurosci.

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Afferent activity into the nucleus accumbens (NAc) occurs in bursts of action potentials. However, it is unclear how synapses in this nucleus respond to such bursts, or how these responses are altered by dopamine (DA). I examined the effects of DA on excitatory and inhibitory responses to trains of stimuli in rat NAc slices. Both EPSCs and IPSCs showed use-dependent depression during trains. Although DA inhibited both glutamate and GABA release in the NAc, it differentially inhibited release during trains. The inhibition of IPSCs persisted throughout the train of stimuli, whereas the inhibition of EPSCs progressively diminished. This differential modulation may be explained by a calcium-dependent change in the recovery from depression at the GABA synapses, where DA acts by decreasing Ca 2ϩ entry. Thus, at later stages of sustained stimulation, DA preferentially inhibits GABA release, producing a net excitatory effect during bursts suggesting a mechanism for enhancing the contrast between competing inputs into the NAc, as well as for affecting long-term plasticity in this structure.

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Section: Discussionsupporting

confidence: 71%

Dopamine Excites Nucleus Accumbens Neurons through the Differential Modulation of Glutamate and GABA Release

Hjelmstad¹

2004

J. Neurosci.

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“…Inhibition mediated by GABA, receptors is very powerful in neocortex (Connors et al, 1988), and IPSPs are strongly engaged by the conditioning stimuli normally used to induce LTP Numerous reports show that the induction of LTP can be facilitated by suppressing GABA, receptor-mediated inhibition with a drug such as BMI (e.g., Wigstrom and Gustafsson, 1983;Kanter and Haberly, 1992). In order to avoid the epileptiform activity that follows even very low doses of BMI in neocortex (Chagnac-Amitai and Connors, 1989) we used a method previously described for visual cortex ; BMI was applied to a very limited area by placing it into the recording pipette and allowing it to leak out slowly but continuously.…”

Section: Ltp In Granular Cortexmentioning

confidence: 99%

Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex

1995

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We have studied vertical synaptic pathways in two cytoarchitectonically distinct areas of rat neocortex--the granular primary somatosensory (SI) area and the agranular primary motor (MI) area--and tested their propensity to generate long-term potentiation (LTP), long-term depression (LTD), and related forms of synaptic plasticity. Extracellular and intracellular responses were recorded in layer II/III of slices in vitro while stimulating in middle cortical layers (in or around layer IV). Under control conditions, 5 Hz theta-burst stimulation produced LTP in the granular area, but not in the agranular area. Agranular cortex did generate short-term potentiation that decayed within 20 min. Varying the inter-burst frequency from 2 Hz to 10 Hz reliably yielded LTP of 21–34% above control levels in granular cortex, but no lasting changes were induced in agranular cortex. However, the agranular cortex was capable of generating LTP if a GABAA receptor antagonist was applied locally at the recording site during the induction phase. In contrast to LTP, an identical form of homosynaptic LTD could be induced in both granular and agranular areas by applying low frequency stimulation (1 Hz for 15 min) to the middle layers. Under control conditions, both LTP and LTD were synapse- specific; theta-burst or low-frequency stimulation in the vertical pathway did not induce changes in responses to stimulation of a layer II/III horizontal pathway. Application of the NMDA receptor antagonist D-2-amino-5-phosphonovaleric acid (AP5) blocked the induction of both LTP and LTD in granular and agranular cortex. In the presence of AP5, low-frequency conditioning stimuli yielded a short-term depression in both areas that decayed within 10–15 min. Nifedipine, which blocks L- type, voltage-sensitive calcium channels, slightly depressed the magnitudes of LTP and LTD but did not abolish them. Synaptic responses evoked during theta-burst stimulation were strikingly different in granular and agranular areas. Responses in granular cortex were progressively facilitated during each sequence of 10 theta-bursts, and from sequence-to-sequence; in contrast, responses in agranular cortex were stable during an entire theta-burst tetanus. The results suggest that vertical pathways in primary somatosensory cortex and primary motor cortex express several forms of synaptic plasticity. They were equally capable of generating LTD, but the pathways in somatosensory cortex much more reliably generated LTP, unless inhibition was reduced. LTP may be more easily produced in sensory cortex because of the pronounced synaptic facilitation that occurs there during repetitive stimulation of the induction phase.

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“…For recording of mIPSCs, potassium gluconate was replaced by KCl (140 mM) in the internal solution, and TTX (0.5 μM), CNQX (10 μM), and AP5 (25 μM) were added in the bath. Series resistance (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) or input resistance (300-500 MΩ) was monitored throughout the wholecell recording and data were discarded if the resistance changed by more than 20%. All recordings were performed at 33 ± 1°C by using an automatic temperature controller (Warner Ins.…”

Section: Electrophysiologymentioning

confidence: 99%

Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons

Liu

Poo

2005

Nature

265

315

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Drugs of abuse are known to cause persistent modification of neural circuits, leading to addictive behaviours 1-5 . Changes in synaptic plasticity in dopamine neurons of the ventral tegmental area (VTA) may contribute to circuit modification induced by many drugs of abuse, including cocaine 6-13 . Here we report that, following repeated cocaine exposure in vivo, excitatory synapses to VTA dopamine neurons become highly susceptible to the induction of long-term potentiation (LTP) by correlated pre-and postsynaptic activity, and this facilitated LTP induction is caused by cocaine-induced reduction of GABA A receptor-mediated inhibition of these dopamine neurons. In midbrain slices from saline-or single cocaine-treated rats LTP could not be induced in VTA dopamine neurons unless GABAergic inhibition was reduced by bicuculline or picrotoxin. In slices from repeated cocaine-treated rats, however, LTP became readily inducible, but was prevented by enhancing GABAergic inhibition with diazepam. Furthermore, repeated cocaine exposure reduced the amplitude of GABAergic synaptic currents and increased the probability of spike initiation in these dopamine neurons. This cocaine-induced enhancement of synaptic plasticity in VTA may be important for the formation of drug-associated memory.To determine the impact of in vivo cocaine exposure on synaptic plasticity in VTA dopamine neurons, we examined LTP induction in these neurons in midbrain slices prepared from rats that were given single (1 d) or repeated (5-7 d) daily intraperitoneal injections of saline or cocaine. The effectiveness of the cocaine treatment was shown by the sensitization of locomotor activity ( Supplementary Fig. 1). Dopamine neurons were identified by the presence of large I h currents and distinct firing characterics 14,15 ( Supplementary Fig. 2). Extracellular stimulation was applied to the rostral region of VTA and evoked excitatory postsynaptic potentials (EPSPs) were monitored by whole-cell recordings from these dopamine neurons at −70 mV, near the reversal potential (−69.7 ± 1.5 mV, n = 5) of inhibitory postsynaptic currents (IPSCs). These EPSPs were mediated by the activation of glutamate receptors, since they were completely abolished by CNQX (6-cyaon-7-nitroquinoxaline-2,3-dione, 20 μM) and AP5 (D-2-amino-5-phosphonopentanoic acid, 50 μM), the antagonist of α-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors (AMPARs) and N-methyl-d-aspartate receptors (NMDARs), respectively. To induce LTP, we used a spike-timing protocol consisting of bursts of EPSP-spike pairs, with the onset of EPSPs preceding the peak of the postsynaptic spike by ∼5 ms (Fig. 1a, see Methods). This pattern of stimulation was used to mimic bursts of spikes observed in VTA dopamine neurons of behaving rats or monkeys in response to reward-related stimuli 16,17 . We found that repetitive EPSP-spike pairing induced a long-lasting increase in the amplitude of EPSPs in VTA dopamine neurons in slices obtained from rats treated with cocaine for 5-7 d (Fig. 1c), but not fr...

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Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition

Cited by 330 publications

References 21 publications

Dopamine Excites Nucleus Accumbens Neurons through the Differential Modulation of Glutamate and GABA Release

Dopamine Excites Nucleus Accumbens Neurons through the Differential Modulation of Glutamate and GABA Release

Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex

Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons

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