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The Journal of Neuroscience, August 10, 2005, 25(32):7366-7376; doi:10.1523/JNEUROSCI.0899-05.2005

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Behavioral/Systems/Cognitive
Coupled Networks of Parvalbumin-Immunoreactive Interneurons in the Rat Basolateral Amygdala

Jay F. Muller, Franco Mascagni, and Alexander J. McDonald

Department of Pharmacology, Physiology, and Neuroscience, University of South Carolina School of Medicine, Columbia, South Carolina 29208

Recent studies indicate that the basolateral amygdala exhibits fast rhythmic oscillations during emotional arousal, but the neuronal mechanisms underlying this activity are not known. Similar oscillations in the cerebral cortex are generated by a network of parvalbumin (PV)-immunoreactive interneurons interconnected by chemical synapses and dendritic gap junctions. The present immunoelectron microscopic study revealed that the basolateral amygdalar nucleus (BLa) contains a network of parvalbumin-immunoreactive (PV+) interneurons interconnected by chemical synapses, dendritic gap junctions, and axonal gap junctions. Twenty percent of synapses onto PV+ neurons were formed by PV+ axon terminals. All of these PV+ synapses were symmetrical. PV+ perikarya exhibited the greatest incidence of PV+ synapses (30%), with lower percentages associated with PV+ dendrites (15%) and spines (25%). These synapses comprised half of all symmetrical synapses formed with PV+ cells. A total of 18 dendrodendritic gap junctions between PV+ neurons were observed, mostly involving secondary and more distal dendrites (0.5-1.0 µm thick). Dendritic gap junctions were often in close proximity to PV+ chemical synapses. Six gap junctions were observed between PV+ axon terminals. In most cases, one or both of these terminals formed synapses with the perikarya of principal neurons. This is the first study to describe dendritic gap junctions interconnecting PV+ interneurons in the basolateral amygdala. It also provides the first documentation of gap junctions between interneuronal axon terminals in the mammalian forebrain. These data provide the anatomical basis for a PV+ network that may play a role in the generation of rhythmic oscillations in the BLa during emotional arousal.

Key words: GABAergic interneurons; chemical synapses; dendritic gap junctions; axonal gap junctions; oscillations; electron microscopy

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Received March 7, 2005; revised June 30, 2005; accepted June 30, 2005.

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