Major dorsoventral differences in the modulation of the local CA1 hippocampal network by NMDA, mGlu5, adenosine A2A and cannabinoid CB1 receptors

Kouvaros, Stylianos; Papatheodoropoulos, Costas

doi:10.1016/j.neuroscience.2015.12.059

Cited by 22 publications

(25 citation statements)

References 128 publications

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“…These dorsal and ventral slices were obtained from the same animals ( n = 20) and constituted a sample of the whole population of slices used in this study. In keeping with previous observations (Kouvaros and Papatheodoropoulos, ) we found that the relationships between stimulation current and fEPSP (Fig. B) and between stimulation current and Fv (Fig.…”

Section: Resultssupporting

confidence: 93%

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Theta burst stimulation‐induced LTP: Differences and similarities between the dorsal and ventral CA1 hippocampal synapses

Kouvaros

Papatheodoropoulos

2016

Hippocampus

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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 receptors prevented the LTP induction by the minimal effective TBS and reduced the magnitude of LTP induced by longer TBS. TBS produced a three-fold 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 receptor-dependent and NMDA receptor-independent facilitation, but the facilitation in the VH was only NMDA receptor-dependent. Also, the TBS-associated activity of GABA 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 of the dorsal and the ventral hippocampal segment to single event memory and to emotional memory respectively. © 2016 Wiley Periodicals, Inc.

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Section: Resultssupporting

confidence: 93%

“…In addition, similar in the two segments was also the relationship between Fv and fEPSP (comparison of the twelve groups of fEPSP-Fv values between DH and VH in Fig. 1D, Mann-Whitney U test, P > 0.05) as previously found (Pofantis and Papatheodoropoulos, 2014;Kouvaros and Papatheodoropoulos, 2016).…”

Section: Baseline Measures In Dh and Vhsupporting

confidence: 84%

Theta burst stimulation‐induced LTP: Differences and similarities between the dorsal and ventral CA1 hippocampal synapses

Kouvaros

Papatheodoropoulos

2016

Hippocampus

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“…The activity of A 2A receptors regulates the function of NMDA receptors in the striatum (Wirkner et al, 2004) and plays a permissive role in the positive interaction between metabotropic glutamate receptors 5 (mGlu 5 receptors) and NMDA receptors in the hippocampus (Tebano et al, 2005;Sarantis et al, 2015;Kouvaros and Papatheodoropoulos, 2016;Krania et al, 2018), an action recently shown to be involved in synaptic plasticity deregulation under conditions of presynaptic A 2A receptor overexpression (Temido-Ferreira et al, 2018). A 2A receptors' activity is also required to gate a form of LTP mediated by postsynaptic NMDA receptors at mossy fibre hippocampal synapses (Rebola et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Adenosine A_2A receptors facilitate synaptic NMDA currents in CA1 pyramidal neurons

Mouro

Rombo

Dias

et al. 2018

British J Pharmacology

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Background and PurposeNMDA receptors play a key role in both synaptic plasticity and neurodegeneration. Adenosine is an endogenous neuromodulator and through membrane receptors of the A2A subtype can influence both synaptic plasticity and neuronal death. The present work was designed to evaluate the influence of adenosine A2A receptors upon NMDA receptor activity in CA1 hippocampal neurons. We discriminated between modulation of synaptic versus extrasynaptic receptors, since extrasynaptic NMDA receptors are mostly associated with neurodegeneration while synaptic NMDA receptors are linked to plasticity phenomena.Experimental ApproachWhole‐cell patch‐clamp recordings were obtained to evaluate NMDA receptor actions on CA1 pyramidal neurons of young adult (5–10 weeks) male Wistar rat hippocampus.Key ResultsActivation of A2A receptors with CGS 21680 (30 nM) consistently facilitated chemically‐evoked NMDA receptor‐currents (NMDA‐PSCs) and afferent‐evoked NMDA‐currents (NMDA‐EPSCs), an action prevented by an A2A receptor antagonist (SCH58261, 100 nM) and a PKA inhibitor, H‐89 (1 μM). These actions did not reflect facilitation in glutamate release since there was no change in NMDA‐EPSCs paired pulse ratio. A2A receptor actions were lost in the presence of an open‐channel NMDA receptor blocker, MK‐801 (10 μM), but persisted in the presence of memantine, at a concentration (10 μM) known to preferentially block extrasynaptic NMDA receptors.Conclusion and ImplicationsThese results show that A2A receptors exert a positive postsynaptic modulatory effect over synaptic, but not extrasynaptic, NMDA receptors in CA1 neurons and, therefore, under non‐pathological conditions may contribute to shift the dual role of NMDA receptors towards enhancement of synaptic plasticity.

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“…DH and VH have different gene expression and a different arrangement of various receptor systems (Witter, ; Moser and Moser, ; Monory et al, ; Dong et al, ; Strange et al, ; Kouvaros and Papatheodoropoulos, ; Lee et al, ; Dubovyk and Manahan‐Vaugham, ) as well as different patterns of plasticity (Papatheodoropoulos and Kostopoulos, ; Maggio and Segal , ; ; Kouvaros and Papatheodoropoulos, ; Dubovyk and Manahan‐Vaughan, ). The adenosine modulation system also differs along the dorsal‐ventral axis of the hippocampus (Moschovos et al, ), with a more effective A 1 R‐mediated control of neurotransmission (Lee et al, ) and excitability in DH (Kim and Johnston, ) and a more evident synergy of A 2A R with metabotropic glutamate receptor 5 to control NMDA receptors in DH (Kouvaros and Papatheodoropoulos, ).…”

mentioning

confidence: 99%

Adenosine A₁ and A_2A receptors differently control synaptic plasticity in the mouse dorsal and ventral hippocampus

Reis

Silva

Almeida

et al. 2019

Journal of Neurochemistry

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The hippocampus is a brain region involved in processing both memory and emotions, through a preferential involvement of the dorsal hippocampus (DH) and ventral hippocampus (VH), respectively. Adenosine A1 and A2A receptors (A1R and A2AR) control both mood and memory, but it is not known if there is a different adenosine modulation of synaptic plasticity along the hippocampal axis. Using adult, C57BL/6 male mice, we show that both A1R and A2AR were more abundant in DH compared with VH. However, recordings of field excitatory postsynaptic potentials at Schaffer collaterals‐CA1 pyramidal synapses revealed that A1R were equi‐effective to inhibit basal excitatory synaptic transmission in DH and VH, but endogenous A1R activation was more effective to depress the probability of release in VH. In contrast, the selective A2AR antagonist (SCH58261, 50 nM) controlled both long‐term potentiation (induced by a high frequency stimulation protocol) and long‐term depression (induced by a low frequency stimulation protocol) selectively in DH rather than VH, whereas the selective A1R antagonist (DPCPX, 100 nM) revealed a similar tonic inhibition of long‐term depression in DH and VH. These findings show a different control of synaptic plasticity by the adenosine modulation system in the dorsal and ventral poles of the hippocampus, which may underlie a different efficiency of the adenosine system to control mood and memory.

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Major dorsoventral differences in the modulation of the local CA1 hippocampal network by NMDA, mGlu5, adenosine A2A and cannabinoid CB1 receptors

Cited by 22 publications

References 128 publications

Theta burst stimulation‐induced LTP: Differences and similarities between the dorsal and ventral CA1 hippocampal synapses

Theta burst stimulation‐induced LTP: Differences and similarities between the dorsal and ventral CA1 hippocampal synapses

Adenosine A_2A receptors facilitate synaptic NMDA currents in CA1 pyramidal neurons

Adenosine A₁ and A_2A receptors differently control synaptic plasticity in the mouse dorsal and ventral hippocampus

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Major dorsoventral differences in the modulation of the local CA1 hippocampal network by NMDA, mGlu5, adenosine A2A and cannabinoid CB1 receptors

Cited by 22 publications

References 128 publications

Theta burst stimulation‐induced LTP: Differences and similarities between the dorsal and ventral CA1 hippocampal synapses

Theta burst stimulation‐induced LTP: Differences and similarities between the dorsal and ventral CA1 hippocampal synapses

Adenosine A2A receptors facilitate synaptic NMDA currents in CA1 pyramidal neurons

Adenosine A1 and A2A receptors differently control synaptic plasticity in the mouse dorsal and ventral hippocampus

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Adenosine A_2A receptors facilitate synaptic NMDA currents in CA1 pyramidal neurons

Adenosine A₁ and A_2A receptors differently control synaptic plasticity in the mouse dorsal and ventral hippocampus