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Dopaminergic enhancement of excitatory synaptic transmission in layer II entorhinal neurons is dependent on D₁-like receptor-mediated signaling.
Neuroscience 2014; 258:74-83N

Abstract

The modulatory neurotransmitter dopamine induces concentration-dependent changes in synaptic transmission in the entorhinal cortex, in which high concentrations of dopamine suppress evoked excitatory postsynaptic potentials (EPSPs) and lower concentrations induce an acute synaptic facilitation. Whole-cell current-clamp recordings were used to investigate the dopaminergic facilitation of synaptic responses in layer II neurons of the rat lateral entorhinal cortex. A constant bath application of 1 μM dopamine resulted in a consistent facilitation of EPSPs evoked in layer II fan cells by layer I stimulation; the size of the facilitation was more variable in pyramidal neurons, and synaptic responses in a small group of multiform neurons were not modulated by dopamine. Isolated inhibitory synaptic responses were not affected by dopamine, and the facilitation of EPSPs was not associated with a change in paired-pulse facilitation ratio. Voltage-clamp recordings of α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) glutamate receptor-mediated excitatory postsynaptic currents (EPSCs) were facilitated by dopamine, but N-methyl-D-aspartate receptor-mediated currents were not. Bath application of the dopamine D₁-like receptor blocker SCH23390 (50 μM), but not the D₂-like receptor blocker sulpiride (50 μM), prevented the facilitation, indicating that it is dependent upon D₁-like receptor activation. Dopamine D₁ receptors lead to activation of protein kinase A (PKA), and including the PKA inhibitor H-89 or KT 5720 in the recording pipette solution prevented the facilitation of EPSCs. PKA-dependent phosphorylation of inhibitor 1 or the dopamine- and cAMP-regulated protein phosphatase (DARPP-32) can lead to a facilitation of AMPA receptor responses by inhibiting the activity of protein phosphatase 1 (PP1) that reduces dephosphorylation of AMPA receptors, and we found here that inhibition of PP1 occluded the facilitatory effect of dopamine. The dopamine-induced facilitation of AMPA receptor-mediated synaptic responses in layer II neurons of the lateral entorhinal cortex is therefore likely mediated via a D₁ receptor-dependent increase in PKA activity and a resulting inhibition in PP1-dependent dephosphorylation of AMPA receptors.

Authors+Show Affiliations

Center for Studies in Behavioral Neurobiology, Department of Psychology, Concordia University, Montréal, Québec H4B 1R6, Canada.Center for Studies in Behavioral Neurobiology, Department of Psychology, Concordia University, Montréal, Québec H4B 1R6, Canada.Center for Studies in Behavioral Neurobiology, Department of Psychology, Concordia University, Montréal, Québec H4B 1R6, Canada. Electronic address: andrew.chapman@concordia.ca.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

24220689

Citation

Glovaci, I, et al. "Dopaminergic Enhancement of Excitatory Synaptic Transmission in Layer II Entorhinal Neurons Is Dependent On D₁-like Receptor-mediated Signaling." Neuroscience, vol. 258, 2014, pp. 74-83.
Glovaci I, Caruana DA, Chapman CA. Dopaminergic enhancement of excitatory synaptic transmission in layer II entorhinal neurons is dependent on D₁-like receptor-mediated signaling. Neuroscience. 2014;258:74-83.
Glovaci, I., Caruana, D. A., & Chapman, C. A. (2014). Dopaminergic enhancement of excitatory synaptic transmission in layer II entorhinal neurons is dependent on D₁-like receptor-mediated signaling. Neuroscience, 258, pp. 74-83. doi:10.1016/j.neuroscience.2013.10.076.
Glovaci I, Caruana DA, Chapman CA. Dopaminergic Enhancement of Excitatory Synaptic Transmission in Layer II Entorhinal Neurons Is Dependent On D₁-like Receptor-mediated Signaling. Neuroscience. 2014 Jan 31;258:74-83. PubMed PMID: 24220689.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Dopaminergic enhancement of excitatory synaptic transmission in layer II entorhinal neurons is dependent on D₁-like receptor-mediated signaling. AU - Glovaci,I, AU - Caruana,D A, AU - Chapman,C A, Y1 - 2013/11/09/ PY - 2013/06/21/received PY - 2013/10/11/revised PY - 2013/10/30/accepted PY - 2013/11/14/entrez PY - 2013/11/14/pubmed PY - 2014/9/30/medline KW - (2R)-amino-5-phosphonopentanoate KW - 2-[4-(2-hydroxyethyl)piperazin-1-yl]ethanesulfonic acid KW - 7-nitro-2,3-dioxo-1,4-dihydroquinoxaline-6-carbonitrile KW - ACSF KW - AMPA KW - APV KW - CNQX KW - DARPP-32 KW - EGTA KW - EPSC KW - EPSP KW - HEPES KW - N-methyl-d-aspartate KW - NMDA KW - PKA KW - PP1 KW - PP2A KW - artificial cerebrospinal fluid KW - dopamine KW - dopamine- and cyclic AMP-regulated phosphoprotein KW - entorhinal cortex KW - ethylene glycol tetraacetic acid KW - excitatory postsynaptic current KW - excitatory postsynaptic potential KW - protein kinase A KW - protein phosphatase 1 KW - protein phosphatase 2A KW - α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid SP - 74 EP - 83 JF - Neuroscience JO - Neuroscience VL - 258 N2 - The modulatory neurotransmitter dopamine induces concentration-dependent changes in synaptic transmission in the entorhinal cortex, in which high concentrations of dopamine suppress evoked excitatory postsynaptic potentials (EPSPs) and lower concentrations induce an acute synaptic facilitation. Whole-cell current-clamp recordings were used to investigate the dopaminergic facilitation of synaptic responses in layer II neurons of the rat lateral entorhinal cortex. A constant bath application of 1 μM dopamine resulted in a consistent facilitation of EPSPs evoked in layer II fan cells by layer I stimulation; the size of the facilitation was more variable in pyramidal neurons, and synaptic responses in a small group of multiform neurons were not modulated by dopamine. Isolated inhibitory synaptic responses were not affected by dopamine, and the facilitation of EPSPs was not associated with a change in paired-pulse facilitation ratio. Voltage-clamp recordings of α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) glutamate receptor-mediated excitatory postsynaptic currents (EPSCs) were facilitated by dopamine, but N-methyl-D-aspartate receptor-mediated currents were not. Bath application of the dopamine D₁-like receptor blocker SCH23390 (50 μM), but not the D₂-like receptor blocker sulpiride (50 μM), prevented the facilitation, indicating that it is dependent upon D₁-like receptor activation. Dopamine D₁ receptors lead to activation of protein kinase A (PKA), and including the PKA inhibitor H-89 or KT 5720 in the recording pipette solution prevented the facilitation of EPSCs. PKA-dependent phosphorylation of inhibitor 1 or the dopamine- and cAMP-regulated protein phosphatase (DARPP-32) can lead to a facilitation of AMPA receptor responses by inhibiting the activity of protein phosphatase 1 (PP1) that reduces dephosphorylation of AMPA receptors, and we found here that inhibition of PP1 occluded the facilitatory effect of dopamine. The dopamine-induced facilitation of AMPA receptor-mediated synaptic responses in layer II neurons of the lateral entorhinal cortex is therefore likely mediated via a D₁ receptor-dependent increase in PKA activity and a resulting inhibition in PP1-dependent dephosphorylation of AMPA receptors. SN - 1873-7544 UR - https://www.unboundmedicine.com/medline/citation/24220689/Dopaminergic_enhancement_of_excitatory_synaptic_transmission_in_layer_II_entorhinal_neurons_is_dependent_on_D₁_like_receptor_mediated_signaling_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S0306-4522(13)00936-6 DB - PRIME DP - Unbound Medicine ER -