An Inhibitory Interface Gates Impulse Traffic between the Input and Output Stations of the Amygdala

Abstract

The central amygdaloid nucleus projects to brainstem and hypothalamic nuclei mediating fear responses and receives convergent sensory inputs from the basolateral amygdaloid complex. However, interposed between the basolateral complex and central nucleus is a string of interconnected GABAergic cell clusters, the intercalated cell masses. Here, we analyzed how intercalated neurons influence impulse traffic between the basolateral complex and central nucleus using whole-cell recordings, microstimulation, and local application of glutamate receptor antagonists in brain slices. Our results suggest that intercalated neurons receive glutamatergic inputs from the basolateral complex and generate feedforward inhibition in neurons of the central nucleus. As the position of the recording site was shifted medially, intercalated cells projected to gradually more medial sectors of the central nucleus and were maximally responsive to progressively more medial stimulation sites in the basolateral complex. Thus, there is a lateromedial correspondence between the position of intercalated cells, their projection site in the central nucleus, and the source of their excitatory afferents in the basolateral complex. In addition, basolateral stimulation sites eliciting maximal excitatory responses in intercalated neurons were flanked laterally by sites eliciting prevalently inhibitory responses via the activation of intercalated cells located more laterally. As a result, the feedforward inhibition generated by intercalated neurons and, indirectly, the amplitude of the responses of central neurons could be increased or decreased depending on which combination of amygdala nuclei are activated and in what sequence. Thus, the output of the central nucleus depends not only on the nature and intensity of sensory inputs but also on their timing and origin.

Brief Social Defeat Stress: Long Lasting Effects on Cocaine Taking During a Binge and Zif268 mRNA Expression in the Amygdala and Prefrontal Cortex

“…Interestingly, administration of cocaine in cocaine-dependent individuals reduces the functional activity of amygdaloid neurons, and this inhibition has been suggested to correlate with cocaine craving (Breiter et al, 1997). Electrophysiological studies indicate that infralimbic projection neurons synapse directly onto GABAergic intercalated cells in the CeA (Sesack et al, 1989;Royer et al, 1999;Quirk et al, 2003), which may be the source of amphetamine-induced decreases in functional activation in the CeA as observed herein.…”

Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey

“…In addition, axonal terminals from orbitofrontal cortices targeted the IM. The latter have been shown to gate information exchange between the BL and Ce nuclei in the amygdala, at least in cats (Royer et al, 1999), which likely underlies cognitive processes prior to emotional expression. This pathway appears to be distinct from those involved in the expression of emotions (e.g.…”

Synergistic Interactions between Cannabinoids and Environmental Stress in the Activation of the Central Amygdala

“…For example, GABAergic cells within intercalated cell masses (ICM), which lie at the anatomical interface of the BLA and CeA, generate feedforward inhibition of CeA neurons in response to BLA activation (Royer et al, 1999(Royer et al, , 2000, and are regulated by extrinsic glutamatergic afferents from the prefrontal cortex and dopaminergic afferents from the ventral midbrain (Bissiere et al, 2003;. Therefore, cannabinoid actions within these regions, which are known to occur (French et al, 1997;Gessa et al, 1998;Auclair et al, 2000;Patel and Hillard, 2003), could modulate CeA activity independently of the BLA, via modulation of ICM neuronal activity.…”