Neurogliaform cells of amygdala: a source of slow phasic inhibition in the basolateral complex

• Published in: The Journal of physiology Vol. 590; no. 22; pp. 5611 - 5627
• Main Authors: Mańko, Mirosława, Bienvenu, Thomas C.M., Dalezios, Yannis, Capogna, Marco
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 15.11.2012; Wiley Subscription Services, Inc; Blackwell Science Inc
• Subjects: Action Potentials - drug effects; Action Potentials - physiology; Amygdala - cytology; Amygdala - physiology; Animals; Axons - physiology; Axons - ultrastructure; Dendrites - physiology; Dendrites - ultrastructure; GABA Antagonists - pharmacology; GABAergic Neurons - classification; GABAergic Neurons - cytology; GABAergic Neurons - physiology; gamma-Aminobutyric Acid - metabolism; Inhibitory Postsynaptic Potentials; Interneurons - classification; Interneurons - cytology; Interneurons - physiology; Neuronal Plasticity; Neuroscience: Cellular/Molecular; Rats; Rodents; Synapses - physiology; Synaptic Transmission; Theta Rhythm
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2012.236745

Key points •  The amygdala is a key brain structure implicated in processing emotions and is thought to underlie anxiety‐related behaviours. •  Interneurons of the basolateral amygdala provide constant silencing of principal cells, and are proven to be active cellular elements during emotional processing. •  We report here a novel interneuron type of the amygdala, termed neurogliaform cell (NGFC), and study its function by a combination of in vivo and in vitro techniques. •  NGFCs provide a peculiar cell‐to‐cell form of communication via volume transmission of GABA. •  In‐depth analysis of specific neuron type is likely to improve the understanding of amygdala circuits in health and disease.   Synaptic inhibition in the amygdala actively participates in processing emotional information. To improve the understanding of interneurons in amygdala networks it is necessary to characterize the GABAergic cell types, their connectivity and physiological roles. We used a mouse line expressing a green fluorescent protein (GFP) under the neuropeptide Y (NPY) promoter. Paired recordings between presynaptic NPY‐GFP‐expressing (+) cells and postsynaptic principal neurons (PNs) of the basolateral amygdala (BLA) were performed. The NPY‐GFP+ neurons displayed small somata and short dendrites embedded in a cloud of highly arborized axon, suggesting a neurogliaform cell (NGFC) type. We discovered that a NPY‐GFP+ cell evoked a GABAA receptor‐mediated slow inhibitory postsynaptic current (IPSC) in a PN and an autaptic IPSC. The slow kinetics of these IPSCs was likely caused by the low concentration and spillover of extracellular GABA. We also report that NGFCs of the BLA fired action potentials phase‐locked to hippocampal theta oscillations in anaesthetized rats. When this firing was re‐played in NPY+‐NGFCs in vitro, it evoked a transient depression of the IPSCs. Presynaptic GABAB receptors and functional depletion of synaptic vesicles determined this short‐term plasticity. Synaptic contacts made by recorded NGFCs showed close appositions, and rarely identifiable classical synaptic structures. Thus, we report here a novel interneuron type of the amygdala that generates volume transmission of GABA. The peculiar functional mode of NGFCs makes them unique amongst all GABAergic cell types of the amygdala identified so far.