Dopamine facilitates long-term depression of glutamatergic transmission in rat prefrontal cortex.
Using sharp-electrode intracellular recordings, we studied the dopaminergic facilitation of synaptic plasticity in layer I-II afferents--layer V neuron glutamatergic synapses in rat prefrontal cortex in vitro. Tetanic stimulation (100 pulses at 50 Hz, four times at 0.1 Hz) to layer I-II afferents induced N-methyl-D-aspartate receptor-independent long-term depression (>40 min) of the glutamatergic synapses when the stimulation was coupled with a bath-application of dopamine. Tetanic stimulation alone did not induce lasting synaptic changes. Dopamine application alone transiently depressed synaptic responses, which fully recovered within 30 min. Pharmacological analyses with antagonists suggested that dopamine action on either D1-like or D2-like receptors can facilitate the induction of long-term depression. However, results with agonists were not fully consistent with the antagonist results: while a D2 agonist mimicked the facilitatory dopamine effect, D1 agonists failed to mimic the effect. We also analysed the synaptic responses during tetanus and found that dopamine prolongs membrane depolarization during high-frequency inputs. Postsynaptic membrane depolarization is indeed critical for long-term depression induction in the presence of dopamine, since postsynaptic hyperpolarization during tetanus blocked the dopaminergic facilitation of long-term depression induction. Postsynaptic injection of the Ca2+ chelator bis-(o-aminophenoxy)-N,N,N',N'-tetra-acetic acid (100 mM in the electrode) also blocked long-term depression induction. Our results show that dopamine lowers the threshold for long-term depression induction in rat prefrontal glutamatergic transmission. A possible underlying mechanism of this dopaminergic facilitation is the enhancement of postsynaptic depolarization during tetanus by dopamine, which may increase the amount of Ca2+ entry from voltage-gated channels to the level sufficient for plasticity induction.
Otani
S
S
Laboratoire de Neurobiologie et Neuropharmacologie du Développement, Institut des Neurosciences, CNRS Université de Paris VI, Pierre et Marie Curie, France.
Blond
O
O
Desce
J M
JM
Crépel
F
F
D015647:2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine / Q000494:pharmacology; D015763:2-Amino-5-phosphonovalerate / Q000494:pharmacology; D000818:Animals; D001552:Benzazepines / Q000494:pharmacology; D002118:Calcium / Q000378:metabolism; D002614:Chelating Agents / Q000494:pharmacology; D004298:Dopamine / Q000502:physiology*; D018491:Dopamine Agonists / Q000494:pharmacology; D018492:Dopamine Antagonists / Q000494:pharmacology; D004533:Egtazic Acid / Q000031:analogs & derivatives / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018698:Glutamic Acid / Q000502:physiology*; D017774:Long-Term Potentiation / Q000502:physiology*; D008297:Male; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology; D009473:Neuronal Plasticity / Q000502:physiology; D017397:Prefrontal Cortex / Q000737:chemistry / Q000502:physiology*; D019257:Quinpirole / Q000494:pharmacology; D051381:Rats; D017207:Rats, Sprague-Dawley; D017447:Receptors, Dopamine D1 / Q000502:physiology; D017448:Receptors, Dopamine D2 / Q000502:physiology; D016194:Receptors, N-Methyl-D-Aspartate / Q000037:antagonists & inhibitors / Q000502:physiology; D013469:Sulpiride / Q000494:pharmacology; D013570:Synaptic Membranes / Q000737:chemistry / Q000502:physiology; D009435:Synaptic Transmission / Q000187:drug effects / Q000502:physiology*
D001552:Benzazepines; D002614:Chelating Agents; D018491:Dopamine Agonists; D018492:Dopamine Antagonists; D018691:Excitatory Amino Acid Antagonists; D017447:Receptors, Dopamine D1; D017448:Receptors, Dopamine D2; D016194:Receptors, N-Methyl-D-Aspartate; D019257:Quinpirole; D018698:Glutamic Acid; D004533:Egtazic Acid; D015647:2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine; D015763:2-Amino-5-phosphonovalerate; D013469:Sulpiride; C025603:1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid; D002118:Calcium; D004298:Dopamine