Dopamine gates action potential backpropagation in midbrain dopaminergic neurons.
Dopamine is released from both axonal and somatodendritic sites of midbrain dopaminergic neurons in an action potential-dependent manner. In contrast to the majority of central neurons, the axon of dopaminergic neurons typically originates from a dendritic site, suggesting a specialized computational function. Here, we examine the initiation and spread of action potentials in dopaminergic neurons of the substantia nigra pars reticulata and reveal that the displacement of the axon to a dendritic site allows highly compartmentalized electrical signaling. In response to a train of synaptic input, action potentials initiated at axon-bearing dendritic sites formed a variable trigger for invasion to the soma and contralateral dendritic tree, with action potentials often confined to the axon-bearing dendrite. The application of dopamine increased this form of electrical compartmentalization, an effect mediated by a tonic membrane potential hyperpolarization leading to an increased availability of a class of voltage-dependent potassium channel. These data suggest that the release of dopamine from axonal and somatodendritic sites are dissociable, and that dopamine levels within the midbrain are dynamically controlled by the somatodendritic spread of action potentials.
Gentet
Luc J
LJ
Medical Research Council Laboratory of Molecular Biology, Cambridge CB2 2QH, United Kingdom.
Williams
Stephen R
SR
D000200:Action Potentials / Q000187:drug effects / Q000502:physiology; D000818:Animals; D001369:Axons / Q000502:physiology; D003712:Dendrites / Q000502:physiology; D004298:Dopamine / Q000494:pharmacology / Q000502:physiology*; D004594:Electrophysiology; D066298:In Vitro Techniques; D015640:Ion Channel Gating / Q000502:physiology; D008564:Membrane Potentials / Q000502:physiology; D009474:Neurons / Q000502:physiology*; D024642:Potassium Channels, Voltage-Gated / Q000378:metabolism; D051381:Rats; D017208:Rats, Wistar; D013378:Substantia Nigra / Q000502:physiology*; D013569:Synapses / Q000502:physiology
D024642:Potassium Channels, Voltage-Gated; D004298:Dopamine