A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function.
The amygdala is under inhibitory control from the cortex through the activation of local GABAergic interneurons. This inhibition is greatly diminished during heightened emotional states due to dopamine release. However, dopamine excites most amygdala interneurons, suggesting that this dopaminergic gate may be mediated by an unknown subpopulation of interneurons. We hypothesized that this gate is mediated by paracapsular intercalated cells, a subset of interneurons that are innervated by both cortical and mesolimbic dopaminergic afferents. Using transgenic mice that express GFP in GABAergic interneurons, we show that paracapsular cells form a network surrounding the basolateral complex of the amygdala. We found that they provide feedforward inhibition into the basolateral and the central amygdala. Dopamine hyperpolarized paracapsular cells through D1 receptors and substantially suppressed their excitability, resulting in a disinhibition of the basolateral and central nuclei. Suppression of the paracapsular system by dopamine provides a compelling neural mechanism for the increased affective behavior observed during stress or other hyperdopaminergic states.
Marowsky
Anne
A
Institute for Pharmacology and Toxicology, University of Zurich, CH-8057 Zurich, Switzerland.
Yanagawa
Yuchio
Y
Obata
Kunihiko
K
Vogt
Kaspar Emanuel
KE
D000200:Action Potentials / Q000187:drug effects / Q000502:physiology; D000679:Amygdala / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D000818:Animals; D048430:Cell Shape / Q000502:physiology; D002540:Cerebral Cortex / Q000166:cytology / Q000378:metabolism; D003712:Dendrites / Q000187:drug effects / Q000378:metabolism / Q000648:ultrastructure; D004298:Dopamine / Q000378:metabolism* / Q000494:pharmacology; D004644:Emotions / Q000502:physiology; D051676:G Protein-Coupled Inwardly-Rectifying Potassium Channels / Q000378:metabolism; D049452:Green Fluorescent Proteins / Q000378:metabolism; D007395:Interneurons / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D051379:Mice; D018345:Mice, Knockout; D008822:Mice, Transgenic; D009415:Nerve Net / Q000166:cytology / Q000187:drug effects / Q000378:metabolism; D009433:Neural Inhibition / Q000187:drug effects / Q000502:physiology*; D009434:Neural Pathways / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D009924:Organ Culture Techniques; D017447:Receptors, Dopamine D1 / Q000187:drug effects / Q000378:metabolism; D013312:Stress, Physiological / Q000378:metabolism / Q000503:physiopathology; D009435:Synaptic Transmission / Q000187:drug effects / Q000502:physiology; D005680:gamma-Aminobutyric Acid / Q000378:metabolism*
D051676:G Protein-Coupled Inwardly-Rectifying Potassium Channels; D017447:Receptors, Dopamine D1; D049452:Green Fluorescent Proteins; D005680:gamma-Aminobutyric Acid; D004298:Dopamine