Synaptic effects induced by alcohol.
paper
Cited
Public
- Authors
- Lovinger, David M; Roberto, Marisa
- Year
- 2013
- Journal
- Current topics in behavioral neurosciences
- PMID
- 21786203
- DOI
- 10.1007/7854_2011_143
- PMCID
- PMC4791588
Ethanol (EtOH) has effects on numerous cellular molecular targets, and alterations in synaptic function are prominent among these effects. Acute exposure to EtOH activates or inhibits the function of proteins involved in synaptic transmission, while chronic exposure often produces opposing and/or compensatory/homeostatic effects on the expression, localization, and function of these proteins. Interactions between different neurotransmitters (e.g., neuropeptide effects on release of small molecule transmitters) can also influence both acute and chronic EtOH actions. Studies in intact animals indicate that the proteins affected by EtOH also play roles in the neural actions of the drug, including acute intoxication, tolerance, dependence, and the seeking and drinking of EtOH. This chapter reviews the literature describing these acute and chronic synaptic effects of EtOH and their relevance for synaptic transmission, plasticity, and behavior.
Acute and chronic EtOH effects on GABAergic and glutamatergic synaptic transmission. a Schematic diagram of a GABAergic synapse, including presynaptic GPCRs that modulate neurotransmitter release, and postsynaptic ionotropic receptors (located both at synapses and extrasynaptically) that mediate fast synaptic transmission. The predominant presynaptic effect of acute EtOH is potentiation of GABA release (most likely by increasing the probability of vesicle fusion). This presynaptic potentiation may involve neuromodulators such as CRF, and activation of presynaptic GPCRs and downstream signaling pathways. Postsynaptically, EtOH potentiates ionotropic GABAA receptor function. Increases in synaptic GABAAR function prolong synaptic responses, while potentiation of extrasynaptic receptors increases tonic current that affects neuronal excitability, b Changes in GABAergic synapses following chronic EtOH exposure. Presynaptically, the release of GABA is decreased. Alterations in levels of neuromodulators that act on GPCRs, as well as altered function of presynaptic GPCRs may contribute to these changes. Postsynaptically, the subunit composition of GABAARs is altered, often including increased synaptic Ξ±4-containing receptors, and fewer Ξ±1-containing synaptic receptors. Synaptic Ξ±4-containing receptors may be less sensitive to acute EtOH, promoting tolerance to synaptic effect of the drug, c Schematic diagram of a glutamatergic synapse on a dendritic spine, including postsynaptic ionotropic receptors that mediate fast synaptic transmission. The predominant effect of acute EtOH is to inhibit ionotropic glutamate receptor function, and all subclasses of these receptors are sensitive to EtOH inhibition. The most potent effects have been observed at kainate and NMDA receptor subtypes, d Changes in glutamatergic synapses following chronic EtOH exposure. Presynaptically, the release of glutamate is enhanced. Postsynaptically, NMDAR function is increased, most likely due to increased receptor density at the synapse. There is also evidence for increased numbers of NR2B-containing NMDARs. There is also evidence of increased volume of the dendritic spine.
| # | Section | Preview |
|---|---|---|
| 100 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.2 Corticotropin-Releasing Factor Actions in the Central Amygdala | The central amygdala (CeA) contains CRF receptors and abundant CRF-containing fibers (De Souza etβ¦ |
| 101 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.2 Corticotropin-Releasing Factor Actions in the Central Amygdala | CRF1Rs mediate the EtOH-induced augmentation of IPSCs in mouse CeA (Nie et al. 2004; Nie et al.β¦ |
| 102 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.2 Corticotropin-Releasing Factor Actions in the Central Amygdala | New electrophysiological data showed that CRF, like EtOH, also enhances GABAergic transmission inβ¦ |
| 103 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.2 Corticotropin-Releasing Factor Actions in the Central Amygdala | the frequency of GABAR-mediated mIPSCs, and this effect is blocked by CRF1R antagonists (Nie et al.β¦ |
| 104 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.2 Corticotropin-Releasing Factor Actions in the Central Amygdala | Chronic EtOH exposure produces functional adaptation of the CRF system in CeA (Hansson et al. 2006,β¦ |
| 105 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.2 Corticotropin-Releasing Factor Actions in the Central Amygdala | CRF-related peptides serve as hormones and neuromodulators of the stress response and play a role inβ¦ |
| 106 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.3 Corticotropin-Releasing Factor Actions in the Bed Nucleus of the Stria Terminalis | The bed nucleus of the stria terminalis (BNST), a brain region associated with anxiety, has enrichedβ¦ |
| 107 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.3 Corticotropin-Releasing Factor Actions in the Bed Nucleus of the Stria Terminalis | BNST (Olive et al. 2002). Interactions between CRF and GABAergic transmission in BNST have beenβ¦ |
| 108 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.3 Corticotropin-Releasing Factor Actions in the Bed Nucleus of the Stria Terminalis | In the same laboratory, a recent study showed the action of dopamine on cellular and synapticβ¦ |
| 109 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.3 Corticotropin-Releasing Factor Actions in the Bed Nucleus of the Stria Terminalis | Francesconi et al. (2009a, b) investigated the effects of protracted withdrawal from alcohol in theβ¦ |
| 110 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.3 Corticotropin-Releasing Factor Actions in the Bed Nucleus of the Stria Terminalis | of alcohol dependence (Francesconi et al. 2009b). In addition, repeated, but not acute,β¦ |
| 111 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.4 Corticotropin-Releasing Factor Actions in the Basolateral Amygdala | Liu et al. (2004) demonstrated that CRF and its related family of peptides act differentially atβ¦ |
| 112 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.4 Corticotropin-Releasing Factor Actions in the Basolateral Amygdala | within both of these nuclei since application of competitive, selective CRF1 or CRF2 receptorβ¦ |
| 113 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.4 Corticotropin-Releasing Factor Actions in the Basolateral Amygdala | Taken together these data suggest that a dysregulation of the extrahypothalamic CRF function is aβ¦ |
| 114 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.5 Neuropeptide Y | Neuropeptide Y (NPY) is an inhibitory peptide produced in abundance in the hypothalamus, andβ¦ |
| 115 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.5 Neuropeptide Y | NPY is generally co-localized with GABA in inhibitory interneurons. NPY mediates its actions byβ¦ |
| 116 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.5 Neuropeptide Y | 2002) for a review). Y1, Y2, and Y5 receptors, and receptor mRNA are found in the amygdala, and eachβ¦ |
| 117 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.5 Neuropeptide Y | Many in vivo studies point to the involvement of NPY in mediating some of the behavioral effects ofβ¦ |
| 118 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.5 Neuropeptide Y | CeA and medial amygdala, but not the basolateral amygdala (Pandey et al. 2005). Further, virallyβ¦ |
| 119 | 3 Neuropeptide Roles in Acute and Chronic Alcohol Actions β 3.1 Corticotropin-Releasing Factor β 3.1.5 Neuropeptide Y | Electrophysiologic findings suggest that NPY and EtOH have a similar profile of actions (Ehlers etβ¦ |
| Name | Type |
|---|---|
| 2-OH-saclofen local | drug |
| 5-HT1c receptor local | drug |
| 5-HT3 receptor | drug |
| AC7 local | drug |
| AC9 local | drug |
| AC/cAMP formation local | drug |
| Acute ethanol treatment local | phenotype |
| acute EtOH actions local | phenotype |
| acute stress | phenotype |
| acute withdrawal | phenotype |
| addiction | phenotype |
| addictive drinking behavior local | phenotype |
| adenylyl cyclase | drug |
| affective disorders | phenotype |
| alcohol | phenotype |
| Alcohol abuse disorders local | phenotype |
| alcohol and drug dependence local | phenotype |
| alcohol dependence | phenotype |
| alcohol-preferring rats | cohort |
| alcohol relapse | phenotype |
| alcohol self-administration | phenotype |
| alcohol tolerance | phenotype |
| Alcohol Use | phenotype |
| Alcohol Use Disorder | phenotype |
| alcohol withdrawal | phenotype |
| alphaxalone | drug |
| AMPAR | drug |
| AMPA receptor | drug |
| AMPA receptors | drug |
| AMPAR-mediated synaptic responses local | phenotype |
| amygdala | anatomy |
| amygdala LTP local | phenotype |
| animal models | cohort |
| Antagonists local | drug |
| anxiety | phenotype |
| Anxiety-like response local | phenotype |
| Anxiety-like states local | phenotype |
| anxiolytic effect | phenotype |
| AP-2 | drug |
| arcuate nucleus | anatomy |
| astressin 2B local | drug |
| ataxia | phenotype |
| ataxic effect | phenotype |
| baclofen | drug |
| basolateral amygdala | anatomy |
| basolateral amygdala nucleus local | anatomy |
| behavior | phenotype |
| behavioral responses to EtOH local | phenotype |
| benzodiazepines | drug |
| bicuculline | drug |
| Binge-like EtOH drinking local | phenotype |
| BLA | anatomy |
| BNST | anatomy |
| brain | anatomy |
| brain development | phenotype |
| brainstem | anatomy |
| Bretazenil local | drug |
| BZP local | drug |
| C57BL/6J | cohort |
| CA1 | anatomy |
| CA1 pyramidal neurons | anatomy |
| Ca2+ | drug |
| CA3 | anatomy |
| calcium | drug |
| CAM kinase II local | drug |
| cAMP | drug |
| CB1 receptor | drug |
| CeA | anatomy |
| CeAm | anatomy |
| central amygdala | anatomy |
| central amygdala nucleus local | anatomy |
| central nervous system | anatomy |
| cerebellar granule cells | anatomy |
| cerebellum | anatomy |
| CET rats local | cohort |
| CGP 35348 local | drug |
| CGP35348 local | drug |
| CGP 55845A local | drug |
| chronic ethanol exposure | phenotype |
| Chronic EtOH local | drug |
| Chronic EtOH-treated rats local | cohort |
| CLTCL1 | gene |
| CNS | anatomy |
| CNS neurons | phenotype |
| cocaine | phenotype |
| cognition | phenotype |
| compulsive alcohol intake | phenotype |
| Constitutive CRHR1 activation local | phenotype |
| control animals | cohort |
| Control-untreated rats local | cohort |
| cortex | anatomy |
| Cortical membranes local | anatomy |
| cortical neurons | anatomy |
| cortical neurons (culture) local | anatomy |
| corticotrophins local | drug |
| corticotropin-releasing factor | drug |
| CREB1 | gene |
| CRF | drug |
| CRF1R | drug |
| CRF2R | drug |
| CRF antagonist local | drug |
| CRFR antagonist local | drug |
| CRFR antagonists local | drug |
| CRF (rat/human) local | drug |
| CRF receptor local | drug |
| CRFRs local | drug |
| CRH | gene |
| CRHBP | gene |
| CRHR1 | gene |
| CRHR1 knockout mice | cohort |
| CRHR1 sensitization local | phenotype |
| CRHR2 | gene |
| CRHR2 knockout mice local | cohort |
| Cynomolgus macaque local | cohort |
| cynomolgus macaques | cohort |
| cys-loop LGICs local | drug |
| Cystine/glutamate exchanger local | drug |
| DAT knockout mice local | cohort |
| DBA/2 mouse local | cohort |
| Decreased benzodiazepine sensitivity local | phenotype |
| Decreased glutamate uptake local | phenotype |
| Decreased LTP local | phenotype |
| Decreased mIPSC frequency local | phenotype |
| Decreased release probability local | phenotype |
| Decreased sensitivity to benzodiazepines local | phenotype |
| Decreased sensitivity to GABA local | phenotype |
| Dendritic calcium signals local | phenotype |
| Dentate granule cell local | anatomy |
| dentate gyrus | anatomy |
| dependence | phenotype |
| Dependent animals local | cohort |
| Dependent rats local | cohort |
| depression | phenotype |
| diazepam | drug |
| DMCM | drug |
| dopamine | drug |
| dopamine neuron local | phenotype |
| dopaminergic neurons | anatomy |
| dopamine uptake local | phenotype |
| dorsal raphe nucleus | anatomy |
| dorsal striatum | anatomy |
| DRD1 | gene |
| DRD2 | gene |
| drinking | phenotype |
| drug dependence | phenotype |
| drug intake | phenotype |
| Duration of ethanol exposure local | phenotype |
| dysphoria | phenotype |
| Emotion | phenotype |
| endocannabinoids | drug |
| enhanced GABAergic synaptic inhibition local | phenotype |
| epilepsy | phenotype |
| ethanol consumption | phenotype |
| ethanol withdrawal | phenotype |
| EtOH | drug |
| EtOH-dependence local | phenotype |
| EtOH-dependent rat local | cohort |
| EtOH-exposed animals local | cohort |
| EtOH inhibition insensitivity local | phenotype |
| EtOH inhibitory action local | phenotype |
| EtOH potentiation of glycine-activated chloride channels local | phenotype |
| EtOH preference local | phenotype |
| EtOH withdrawal local | phenotype |
| evoked IPSCs local | phenotype |
| Excessive EtOH intake local | phenotype |
| Excitatory postsynaptic currents (EPSCs) local | phenotype |
| excitotoxicity | phenotype |
| extended amygdala | anatomy |
| extracellular 5-HT levels local | phenotype |
| feeding | phenotype |
| flunitrazepam | drug |
| food intake | phenotype |
| forebrain | anatomy |
| forskolin | drug |
| Fyn | gene |
| GABA | phenotype |
| GABAA IPSCs local | phenotype |
| GABA_A_receptor local | drug |
| GABAA receptor | drug |
| GABAA receptor Ξ±1Ξ²2Ξ³2 local | drug |
| GABAA receptor Ξ±4Ξ²2Ξ³2 local | drug |
| GABAAR function local | phenotype |
| GABAB receptor | drug |
| GABAB_receptor local | drug |
| GABAB receptor antagonist | drug |
| GABAB system local | phenotype |
| GABAergic inhibitory transmission local | phenotype |
| GABAergic synapse local | anatomy |
| GABAergic synaptic changes local | phenotype |
| GABAergic tone local | phenotype |
| GABA IPSC amplitude local | phenotype |
| GABA IPSCs local | phenotype |
| GABA levels local | phenotype |
| Gabbr1 | gene |
| Gabra1 | gene |
| GABRA2 | gene |
| GABRA3 | gene |
| Gabra4 | gene |
| GABRA5 | gene |
| GABRA6 | gene |
| GABRB | gene |
| GABRB1 | gene |
| Gabrb2 | gene |
| Gabrb3 | gene |
| Gabrd | gene |
| GABRG | gene |
| Gabrg1 | gene |
| Gabrg2 | gene |
| GDP | drug |
| gene transcription | phenotype |
| Gi/o G protein class local | drug |
| GIRK potassium channel local | drug |
| glutamate | drug |
| Glutamate receptor | drug |
| glutamatergic EPCS local | phenotype |
| glutamatergic system | drug |
| glycine | drug |
| glycine receptor | drug |
| GlyR | drug |
| GPCRs local | drug |
| G protein local | drug |
| G protein-coupled receptor (GPCR) superfamily local | drug |
| G protein Ξ± subunit local | drug |
| G protein Ξ² subunit local | drug |
| G protein Ξ³ subunit local | drug |
| Gq-like G protein class local | drug |
| Gq-like Ξ± subunits local | drug |
| Gq-subclass local | drug |
| GRIA local | gene |
| GRIA1 | gene |
| GRIA2 | gene |
| GRIA3 | gene |
| GRIK local | gene |
| GRIN local | gene |
| GRIN1 | gene |
| GRIN1 splice variant local | variant |
| GRIN2A | gene |
| GRIN2B | gene |
| GRIN2C | gene |
| GRIN3A | gene |
| GRM1 | gene |
| Gs-like G protein local | drug |
| Gs-like G protein class local | drug |
| GTP | drug |
| HCN1 local | gene |
| high EtOH consumption local | phenotype |
| hippocampal CA1 region | anatomy |
| hippocampal formation | anatomy |
| hippocampal neurons | anatomy |
| hippocampal neurons (culture) local | anatomy |
| hippocampus | anatomy |
| HPA_axis_signaling local | phenotype |
| human | cohort |
| human alcoholics | phenotype |
| hyperalgesia | phenotype |
| hyper-excitability local | phenotype |
| hyperexcitable CNS state local | phenotype |
| hyperpolarization | phenotype |
| hypoglossal nucleus local | anatomy |
| hypothalamus | anatomy |
| Increased 3H-bicuculline binding site density local | phenotype |
| Increased 3H-GABA release local | phenotype |
| Increased contribution of NMDARs to glutamatergic transmission local | phenotype |
| Increased CRHR1 receptor number local | phenotype |
| Increased EtOH intake local | phenotype |
| Increased extracellular glutamate levels local | phenotype |
| Increased GABA release local | phenotype |
| Increased GABA transmission local | phenotype |
| Increased GRIN1 splice variant expression local | phenotype |
| Increased mIPSC frequency | phenotype |
| Increased neuronal excitability local | phenotype |
| Increased neurotransmitter release local | phenotype |
| Increased NMDAR expression in dendritic spines local | phenotype |
| Increased NMDAR function local | phenotype |
| Increased NR2A protein expression local | phenotype |
| Increased NR2B protein expression local | phenotype |
| Increased paired-pulse plasticity local | phenotype |
| Increased presynaptic regulation of GABA release local | phenotype |
| Increased sIPSC frequency | phenotype |
| Increased striatal dopamine levels local | phenotype |
| Increased synaptic glutamate release local | phenotype |
| Increased tonic release of CRF local | phenotype |
| inhibition of neurons local | phenotype |
| inositol triphosphate | drug |
| insula | anatomy |
| intoxication | phenotype |
| intracellular calcium | phenotype |
| in vitro brain slices local | anatomy |
| Ion channels local | drug |
| ionotropic glutamate receptor | drug |
| iPSCs | cohort |
| jcBNST local | anatomy |
| kainate receptor | drug |
| kainate receptors local | drug |
| Kcnj6 | gene |
| Key brain regions local | anatomy |
| Lack of tolerance to acute EtOH and flunitrazepam on GABAA IPSCs local | phenotype |
| larger EtOH effect local | phenotype |
| lateral amygdala | anatomy |
| lateral septum | anatomy |
| Lateral septum mediolateral nucleus local | anatomy |
| learning and memory | phenotype |
| long-term depression | phenotype |
| long-term potentiation | phenotype |
| Long_term_potentiation local | phenotype |
| low EtOH sensitivity local | phenotype |
| LSMLN local | anatomy |
| LTD | phenotype |
| LTP | phenotype |
| LTP-IE local | phenotype |
| MAP kinases local | drug |
| medial amygdala | anatomy |
| medial prefrontal cortex | anatomy |
| Medial septum/diagonal band neurons local | anatomy |
| membrane potential | phenotype |
| memory | phenotype |
| metabotropic glutamate receptors | drug |
| Mg2+ | drug |
| mGluR local | drug |
| mGluR1 local | drug |
| mGluR5 | drug |
| mGluR-LTD local | phenotype |
| mice | cohort |
| midbrain | anatomy |
| mIPSC duration local | phenotype |
| mIPSC frequency | phenotype |
| mIPSC frequency (decrease) local | phenotype |
| mIPSCs local | phenotype |
| monoamine levels local | phenotype |
| motor coordination impairment local | phenotype |
| mouse brain | anatomy |
| MTIP | drug |
| muscarinic acetylcholine receptors local | gene |
| Muscarinic_receptor local | drug |
| muscimol | drug |
| Na+ | drug |
| NaΓ―ve control rats local | cohort |
| NaΓ―ve rat local | cohort |
| naive rats local | cohort |
| naΓ―ve rats local | cohort |
| NaΓ―ve rats local | cohort |
| NaΓ―ve rats local | phenotype |
| Negative emotional responses local | phenotype |
| neuroadaptative changes local | phenotype |
| neuronal activity | phenotype |
| neuronal excitability | phenotype |
| neuronal integrity | phenotype |
| neuronal loss | phenotype |
| Neuropeptides local | drug |
| neuroprotection | phenotype |
| neurotransmitter local | drug |
| neurotransmitter release | phenotype |
| nicotinic acetylcholine receptor | drug |
| Nitric oxide signaling local | phenotype |
| NMDA-mediated synaptic transmission local | phenotype |
| NMDAR | drug |
| NMDA receptor | drug |
| NMDAR-mediated synaptic transmission local | phenotype |
| No change in 3H-baclofen binding site density local | phenotype |
| nociceptin | drug |
| Nociceptin opioid receptor local | drug |
| Non-dependent mice local | cohort |
| Non-dependent rats local | cohort |
| NOR local | drug |
| NP rats | cohort |
| NPY | gene |
| NPY1R | gene |
| NPY2R | gene |
| NPY5R | gene |
| NPY KO mice local | cohort |
| NPY overexpressors local | cohort |
| NR2B mRNA upregulation local | phenotype |
| NR2B protein upregulation local | phenotype |
| nucleus accumbens | anatomy |
| nucleus of the solitary tract | anatomy |
| Oprd1 | cohort |
| OPRK1 | cohort |
| OPRL1 | cohort |
| OPRM1 | cohort |
| P2RX3 local | gene |
| P2RX4 local | gene |
| P2X receptor local | drug |
| P2X receptor local | gene |
| paired-pulse facilitation | phenotype |
| paraventricular nucleus | anatomy |
| pentylenetetrazole | drug |
| peripheral nervous system | anatomy |
| pertussis toxin | drug |
| Phospholipase A2 | drug |
| physical dependence | phenotype |
| PKA | drug |
| PKC | gene |
| PKCΞ΅ knockout mice | cohort |
| positive reinforcing effect local | phenotype |
| Postdependent individuals local | cohort |
| postpiriform transition area local | anatomy |
| Postsynaptic response to GABA local | phenotype |
| potassium | drug |
| potassium channels | drug |
| potentiation of GABAA receptor function local | phenotype |
| PPD | phenotype |
| PPF ratio local | phenotype |
| PPF ratio of IPSCs local | phenotype |
| P rats | cohort |
| Presynaptic decrease in GABA release local | phenotype |
| Primary cortical cultures local | anatomy |
| PRKACA | gene |
| PRKCA | gene |
| PRKCD | gene |
| PRKCE | gene |
| PRKCG | gene |
| Protein kinase C | drug |
| protracted abstinence | phenotype |
| protracted withdrawal | phenotype |
| protracted withdrawal from alcohol local | phenotype |
| psychostimulants | drug |
| Purkinje cells | anatomy |
| PVN | anatomy |
| R121919 local | drug |
| rats | cohort |
| receptor desensitization | phenotype |
| Reduced GABA release probability local | phenotype |
| Reduced glutamatergic transmission local | phenotype |
| Reduced LTP local | phenotype |
| relapse | phenotype |
| Relapse-like behaviors local | phenotype |
| Release probability (decrease) local | phenotype |
| reward | phenotype |
| Ro15-4513 | drug |
| RO 15-4513 local | drug |
| Roberto et al. 2004a local | cohort |
| Roberto et al. 2010 local | cohort |
| R-type voltage-gated calcium channel local | drug |
| Saline-treated animals local | cohort |
| Schaffer collateral inputs to CA1 pyramidal neurons local | anatomy |
| sedative effects | phenotype |
| sedatives | drug |
| Seizure induction local | phenotype |
| Seizure susceptibility | phenotype |
| serotonin | drug |
| serotonin3 receptor local | drug |
| serotonin type 2 receptors local | gene |
| severe intoxication local | phenotype |
| short-term plasticity phenomena local | phenotype |
| SLC6A3 | gene |
| Sleep disturbance | phenotype |
| Slow inhibitory postsynaptic potential local | phenotype |
| spinal cord | anatomy |
| SpragueβDawley rat local | cohort |
| stress | phenotype |
| Stress and anxiety local | phenotype |
| Stress-induced anxiogenic-like response local | phenotype |
| stress-induced relapse to cocaine self-administration local | phenotype |
| stress-like effects local | phenotype |
| stress response | phenotype |
| striatum | anatomy |
| tetrodotoxin | drug |
| thalamus | anatomy |
| THIP | drug |
| tolerance | phenotype |
| tonic current | phenotype |
| Tonic GABA current local | phenotype |
| tyrosine kinase local | drug |
| Ucn1 | drug |
| Ucn2 | drug |
| Ucn3 | drug |
| Ucn I local | drug |
| urocortin | drug |
| ventral tegmental area | anatomy |
| Vesicle fusion local | phenotype |
| vlBNST local | anatomy |
| voltage-gated calcium channel | drug |
| Voluntary EtOH drinking local | phenotype |
| VTA | anatomy |
| VTA dopamine neuron local | phenotype |
| water intake | phenotype |
| wild-type mice | cohort |
| Wistar rats | cohort |
| withdrawal | phenotype |
| Withdrawal 48h after EtOH local | phenotype |
| Withdrawal excitability local | phenotype |
| Withdrawal-induced increase in alcohol drinking local | phenotype |
| Xenopus laevis oocyte preparation local | cohort |
| Y1 receptor local | drug |
| Y2 receptor local | drug |
| Y4 receptor local | drug |
| Y5 receptor local | drug |
| Y6 receptor local | drug |
| zolpidem | drug |
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