Morphological and physiological properties of CCK/CB1R-expressing interneurons in the basal amygdala

Principal neurons in cortical regions including the basal nucleus of the amygdala (BA) are innervated by several types of inhibitory cells, one of which expresses the neuropeptide cholecystokinin (CCK) and the type 1 cannabinoid receptor (CB1R). CCK/CB1R-expressing interneurons may have a profound impact on amygdalar function by controlling its output. However, very little is known about their properties, and therefore their role in circuit operation cannot be predicted. To characterize the CCK/CB1R-expressing interneurons in the BA, we combined in vitro electrophysiological recordings and neuroanatomical techniques in a transgenic mouse that expresses DsRed fluorescent protein under the control of the CCK promoter. We found that the majority of CCK/CB1R-positive interneurons expressed either the type 3 vesicular glutamate transporter (VGluT3) or the Ca²⁺ binding protein calbindin (Calb). VGluT3+ CCK/CB1R-expressing interneurons targeted the soma of principal neurons more often than Calb+ CCK/CB1R-expressing interneurons, but the dendritic morphology and membrane properties of these two neurochemically distinct interneuron types were not significantly different. The results of paired recordings showed that the unitary IPSC properties of VGluT3+ or Calb+ CCK/CB1R-expressing interneurons recorded in principal neurons were indistinguishable. We verified that endocannabinoids at the output synapses of CCK/CB1R-expressing interneurons could potently reduce the unitary IPSC magnitude. In summary, independent of the neurochemical content, CCK/CB1R-expressing interneurons have similar physiological and morphological properties, providing an endocannabinoid-sensitive synaptic inhibition onto the amygdalar principal neurons.