L-type Ca2+ channel activity determines modulation of GABA release by dopamine in the substantia nigra reticulata and the globus pallidus of the rat

Recillas‐Morales, Sergio; Sanchez-Vega, Lizzette; Ochoa-Sánchez, N.; Caballero-Florán, Isaac H.; Paz‐Bermúdez, Francisco; Silva, I.; Aceves, Jorge; Erlij, David; Florán, Benjamí­n

doi:10.1016/j.neuroscience.2013.10.037

Cited by 11 publications

(6 citation statements)

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“…Current clamp experiments in slices showed that this is also the case for striatal FSI as well as other neurons [ 37 ]. Ca V 1 also induces short-term synaptic depression and facilitates GABA release in SNr [ 53 , 54 ]. Blockade of enhanced firing by nicardipine shows that Ca V 1 channels are in part responsible for these functions in striatal FSI.…”

Section: Discussionmentioning

confidence: 99%

Calcium currents in striatal fast-spiking interneurons: dopaminergic modulation of CaV1 channels

et al. 2018

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BackgroundStriatal fast-spiking interneurons (FSI) are a subset of GABAergic cells that express calcium-binding protein parvalbumin (PV). They provide feed-forward inhibition to striatal projection neurons (SPNs), receive cortical, thalamic and dopaminergic inputs and are coupled together by electrical and chemical synapses, being important components of the striatal circuitry. It is known that dopamine (DA) depolarizes FSI via D1-class DA receptors, but no studies about the ionic mechanism of this action have been reported. Here we ask about the ion channels that are the effectors of DA actions. This work studies their Ca2+ currents.ResultsWhole-cell recordings in acutely dissociated and identified FSI from PV-Cre transgenic mice were used to show that FSI express an array of voltage gated Ca2+ channel classes: CaV1, CaV2.1, CaV2.2, CaV2.3 and CaV3. However, CaV1 Ca2+ channel carries most of the whole-cell Ca2+ current in FSI. Activation of D1-like class of DA receptors by the D1-receptor selective agonist SKF-81297 (SKF) enhances whole-cell Ca2+ currents through CaV1 channels modulation. A previous block of CaV1 channels with nicardipine occludes the action of the DA-agonist, suggesting that no other Ca2+ channel is modulated by D1-receptor activation. Bath application of SKF in brain slices increases the firing rate and activity of FSI as measured with both whole-cell and Ca2+ imaging recordings. These actions are reduced by nicardipine.ConclusionsThe present work discloses one final effector of DA modulation in FSI. We conclude that the facilitatory action of DA in FSI is in part due to CaV1 Ca2+ channels positive modulation.

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Section: Discussionmentioning

confidence: 99%

Calcium currents in striatal fast-spiking interneurons: dopaminergic modulation of CaV1 channels

et al. 2018

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“…For example, D1R from striatal collaterals stimulates the GABA release by coupling to P/Q type Ca 2+ channels (Arias‐Montano et al., 2007), while striato‐nigral terminals release seems to be related to L type Ca 2+ channels (Recillas‐Morales et al., 2014). This difference also occurs at striato‐pallidal terminals, D2R couple to L‐type Ca 2+ channels (Recillas‐Morales et al., 2014), whereas at striatal collaterals, couple to N‐type Ca 2+ channels (Momiyama & Koga, 2001). Thus, this implies more research to solve these questions.…”

Section: Discussionmentioning

confidence: 99%

“…Part of this effect is modulated by Ca 2+ entry via P/Q-type voltage-gated calcium channels (Deliu et al, 2015). In striato-nigral terminals, P/Q Ca 2+ channels mediate part of the release in this experimental condition (Recillas- Morales et al, 2014); thus, a similar mechanism could occur at nigral terminals. However, the persistence of the LPI effect on release after Ca 2+ stores depletion discards this possibility (Figures 4(d) and 4(e)).…”

Section: External Ca 2+ Dependence Of Gpr55 Effects On [ 3 H]-gaba Re...mentioning

confidence: 95%

Presynaptic nigral GPR55 receptors stimulate [³H]‐GABA release through [³H]‐cAMP production and PKA activation and promote motor behavior

Sánchez‐Zavaleta

Ávalos-Fuentes

González-Hernández

et al. 2022

Synapse

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Striatal medium-sized spiny neurons express mRNA and protein of GPR55 receptors that stimulate neurotransmitter release; thus, GPR55 could be sent to nigral striatal projections, where it might modulate GABA release and motor behavior. Here, we study the presence of GPR55 receptors at striato-nigral terminals, their modulation of GABA release, their signaling pathway, and their effect on motor activity. By double immunohistochemistry, we found the colocation of GPR55 protein and substance P in the dorsal striatum. In slices of the rat substantia nigra, the GPR55 agonists LPI and O-1602 stimulated [ 3 H]-GABA release induced by high K + depolarization in a dose-dependent manner. The antagonists CID16020046 and cannabidiol prevented agonist stimulation in a dose-dependent way. The effect of GPR55 on nigral [ 3 H]-GABA release was prevented by lesion of the striatum with kainic acid, which was accompanied by a decrement of GPR55 protein in nigral synaptosomes, indicating the presynaptic location of receptors. The depletion of internal Ca 2+ stores with thapsigargin did not prevent the effect of LPI on [ 3 H]-GABA release, but the remotion or chelation of external calcium did. Blockade of Gi, Gs, PLC, PKC, or dopamine D1 receptor signaling proteins did not prevent the effect of GPR55 on release. However, the activation of GPR55 stimulated [ 3 H]-cAMP accumulation and PKA activity. Intranigral unilateral injection of LPI induces contralateral turning. This turning was prevented by CID16020046, cannabidiol, and bicuculline but not by SCH 23390. Our data indicate that presynaptic GPR55 receptors stimulate [ 3 H]-GABA release at striato-nigral terminals through [ 3 H]-cAMP production and stimulate motor behavior.

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“…While VTA LTCCs are located post-synaptically on DA cell bodies [5,23], it is possible that isradipine's dopaminergic effects are instead mediated by pre-synaptic LTCCs. Recent evidence revealed the ability of LTCC activation and blockade in the substantia nigra reticulata to increase and decrease GABA release, respectively-effects suggested to be mediated by LTCCs on GABA terminals [24]. If presynaptic LTCCs are also present on GABA terminals in the VTA, one would predict that isradipine infusion could decrease VTA inhibitory tone to facilitate enhanced DA activity and downstream DA release.…”

Section: Discussionmentioning

confidence: 99%

The L-type calcium channel blocker, isradipine, attenuates cue-induced cocaine-seeking by enhancing dopaminergic activity in the ventral tegmental area to nucleus accumbens pathway

Addy

Nunes

Hughley

et al. 2018

Neuropsychopharmacol

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Previous preclinical and clinical investigations have focused on the L-type calcium channel (LTCC) as a potential therapeutic target for substance abuse. While some clinical studies have examined the ability of LTCC blockers to alter cocaine's subjective effects, very few LTCC studies have examined cocaine relapse. Here, we examined whether ventral tegmental area (VTA)-specific or systemic administration of the LTCC inhibitor, isradipine, altered cocaine-seeking behavior in a rat model. Male Sprague-Dawley rats first received 10 days of cocaine self-administration training (2 h sessions), where active lever depression resulted in delivery of a ∼0.5 mg/kg cocaine infusion paired with a tone + light cue. Rats then underwent 10 days of forced abstinence, without access to cocaine or cocaine cues. Rats were then returned to the opertant chamber for the cue-induced cocaine-seeking test, where active lever depression in the original training context resulted in tone + light cue presentation. We found VTA specific or systemic isradipine administration robustly attenuated cocaine-seeking, without altering cocaine-taking nor natural reward seeking. Dopamine (DA) signaling in the nucleus accumbens (NAc) core is necessary and sufficient for cue-induced drug-seeking. Surprisingly in our study, isradipine enhanced tonic and phasic DA signaling in cocaine abstinent rats, with no change in sucrose abstinent nor naïve rats. Strikingly, isradipine's behavioral effects were dependent upon NAc core DA receptor activation. Together, our findings reveal a novel mechanism by which the FDA-approved drug, isradipine, could act to decrease cocaine relapse.

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L-type Ca2+ channel activity determines modulation of GABA release by dopamine in the substantia nigra reticulata and the globus pallidus of the rat

Cited by 11 publications

References 50 publications

Calcium currents in striatal fast-spiking interneurons: dopaminergic modulation of CaV1 channels

Calcium currents in striatal fast-spiking interneurons: dopaminergic modulation of CaV1 channels

Presynaptic nigral GPR55 receptors stimulate [³H]‐GABA release through [³H]‐cAMP production and PKA activation and promote motor behavior

The L-type calcium channel blocker, isradipine, attenuates cue-induced cocaine-seeking by enhancing dopaminergic activity in the ventral tegmental area to nucleus accumbens pathway

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L-type Ca2+ channel activity determines modulation of GABA release by dopamine in the substantia nigra reticulata and the globus pallidus of the rat

Cited by 11 publications

References 50 publications

Calcium currents in striatal fast-spiking interneurons: dopaminergic modulation of CaV1 channels

Calcium currents in striatal fast-spiking interneurons: dopaminergic modulation of CaV1 channels

Presynaptic nigral GPR55 receptors stimulate [3H]‐GABA release through [3H]‐cAMP production and PKA activation and promote motor behavior

The L-type calcium channel blocker, isradipine, attenuates cue-induced cocaine-seeking by enhancing dopaminergic activity in the ventral tegmental area to nucleus accumbens pathway

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Presynaptic nigral GPR55 receptors stimulate [³H]‐GABA release through [³H]‐cAMP production and PKA activation and promote motor behavior