Large intercalated neurons of amygdala relay noxious sensory information.

T. C. M. Bienvenu, D. Busti, B. R. Micklem, M. Mansouri, P. J. Magill, F. Ferraguti, M. Capogna
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.


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