The intercalated nuclear complex of the primate amygdala

Published in final edited form as: Neuroscience. 2016 August 25; 330: 267–290. doi:10.1016/j.neuroscience.2016.05.0.The organization of the inhibitory intercalated cell masses (IM) of the primate amygdala is largely unknown despite their key role in emotional processes. We studied the structural, topographic, neurochemical and intrinsic connectional features of IM neurons in the rhesus monkey brain. We found that the intercalated neurons are not confined to discrete cell clusters, but form a neuronal net that is interposed between the basal nuclei and extends to the dorsally located anterior, central, and medial nuclei of the amygdala. Unlike the IM in rodents, which are prominent in the anterior half of the amygdala, the primate inhibitory net stretched throughout the antero-posterior axis of the amygdala, and was most prominent in the central and posterior extent of the amygdala. There were two morphologic types of intercalated neurons: spiny and aspiny. Spiny neurons were the most abundant; their somata were small or medium size, round or elongated, and their dendritic trees were round or bipolar, depending on location. The aspiny neurons were on average slightly larger and had varicose dendrites with no spines. There were three non-overlapping neurochemical populations of IM neurons, in descending order of abundance: (1) Spiny neurons that were positive for the striatal associated dopamine- and cAMP-regulated phosphoprotein (DARPP-32+); (2) Aspiny neurons that expressed the calcium-binding protein calbindin (CB+); and (3) Aspiny neurons that expressed nitric oxide synthase (NOS+). The unique combinations of structural and neurochemical features of the three classes of IM neurons suggest different physiological properties and function. The three types of IM neurons were intermingled and likely interconnected in distinct ways, and were innervated by intrinsic neurons within the amygdala, or by external sources, in pathways that underlie fear conditioning and anxiety.We thank Dr. Alan Peters for EM consultation, Dr. John Fiala for assistance in adapting the free 3D-reconstruction software he developed, Drs. Ron Killiany, Maria Medalla and Clare Timbie for MRI and surgical assistance, Drs. Paul Greengard and Jean-Antoine Girault for their generous gift of the DARPP-32 antibody, and Mrs. Marcia Feinberg for exceptional technical assistance and imaging at the electron microscope. Supported by grants from NIH (BZ: R01 MH101209, HB: R01 MH057414, R01 NS024760) and NSF CELEST (YJ, HB, BZ: 0835976). (R01 MH101209 - NIH; R01 MH057414 - NIH; R01 NS024760 - NIH; 0835976 - NSF CELEST)Accepted manuscrip