Large intercalated neurons of amygdala relay noxious sensory information.
Journal of Neuroscience. 2015-02-04; 35(5): 2044-2057
DOI: 10.1523/jneurosci.1323-14.2015
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Various GABAergic neuron types of the amygdala cooperate to control principal
cell firing during fear-related and other behaviors, and understanding their
specialized roles is important. Among GABAergic neurons, the so-called
intercalated cells (ITCcs) are critically involved in the expression and
extinction of fear memory. Tightly clustered small-sized spiny neurons constitute
the majority of ITCcs, but they are surrounded by sparse, larger neurons
(L-ITCcs) for which very little information is known. We report here a detailed
neurochemical, structural and physiological characterization of rat L-ITCcs, as
identified with juxtacellular recording/labeling in vivo. We supplement these
data with anatomical and neurochemical analyses of nonrecorded L-ITCcs. We
demonstrate that L-ITCcs are GABAergic, and strongly express metabotropic
glutamate receptor 1α and GABAA receptor α1 subunit, together with moderate
levels of parvalbumin. Furthermore, L-ITCcs are innervated by fibers enriched
with metabotropic glutamate receptors 7a and/or 8a. In contrast to small-sized
spiny ITCcs, L-ITCcs possess thick, aspiny dendrites, have highly branched,
long-range axonal projections, and innervate interneurons in the basolateral
amygdaloid complex. The axons of L-ITCcs also project to distant brain areas,
such as the perirhinal, entorhinal, and endopiriform cortices. In vivo recorded
L-ITCcs are strongly activated by noxious stimuli, such as hindpaw pinches or
electrical footshocks. Consistent with this, we observed synaptic contacts on
L-ITCc dendrites from nociceptive intralaminar thalamic nuclei. We propose that,
during salient sensory stimulation, L-ITCcs disinhibit local and distant
principal neurons, acting as “hub cells,” to orchestrate the activity of a
distributed network.