Cholecystokinin immunoreactive neurons in the basolateral amygdala of the rhesus monkey (Macaca mulatta)

Abstract

Several distinct subpopulations of interneurons (INs) in the amygdalar basolateral nuclear complex (BNC) of the rat can be recognized on the basis of their expression of calcium‐binding proteins and neuropeptides, including parvalbumin (PV), somatostatin (SOM), calretinin (CR), and cholecystokinin (CCK). In the rat BNC CCK is expressed in two separate IN subpopulations, termed large (CCKL) and small (CCKS). These subpopulations exhibit distinct connections indicative of discrete functional roles in the circuitry of the BNC. Although there have been several studies of PV+, SOM+, and CR+ INs in the primate BNC, there is almost no information regarding CCK+ INs in these species. Therefore, in the present study the distribution and morphology of CCK+ INs and their axon terminals in the BNC of the monkey was investigated. CCK immunoreactivity in the BNC was observed in somata and proximal dendrites of nonpyramidal neurons, as well as in axon terminals. A moderate density of CCK+ INs was found in all nuclei of the BNC. CCK+ INs in the BNC were morphologically heterogeneous, with both small and large varieties observed. All CCK+ somata gave rise to 2–4 dendrites that branched sparingly and were aspiny. CCK+ axon terminals in the BNC were found both in the neuropil and forming pericellular baskets contacting somata of pyramidal cells. In addition, many CCK+ neurons were contacted by multiple CCK+ terminals, indicative of the existence of a CCK interneuronal network. These data indicate that the morphology of CCK+ INs in the monkey is very similar to that of the rat.

Interneuron Types and Their Circuits in the Basolateral Amygdala

“…In the BLA, CCK/CB1 basket cells are also present both in the rodent (Katona et al, 2001 ; McDonald and Mascagni, 2001 ; Vereczki et al, 2016 ; Rovira-Esteban et al, 2017 ) and in the monkey (McDonald, 2021 ), giving rise to 0.9% of all neurons in the LA and 2.1% in the BA in the mouse BLA (Vereczki et al, 2021 ). CCK/CB1 basket cells typically have large somata and multipolar dendritic trees both in rodents (Mascagni and McDonald, 2003 ; Vereczki et al, 2016 ; Rovira-Esteban et al, 2017 ) and monkey (McDonald and Mascagni, 2019 ). The neurochemical content of CCK/CB1 basket cells is variable, as they may express vesicular glutamate transporter type 3 (VGluT3) and Calb in largely non-overlapping subpopulations (Omiya et al, 2015 ; Rovira-Esteban et al, 2017 ).…”

Neuronal localization of m1 muscarinic receptor immunoreactivity in the monkey basolateral amygdala

“…Electron microscopic studies in rat have demonstrated that 10% of m1R+ axon terminals in the BNC form symmetrical synapses. The main postsynaptic targets of these m1R+ axon terminals are somata, axon initial segments, and thick proximal dendrites of PNs, which are the same structures targeted by many GABAergic INs, especially PV and CCK INs (McDonald et al, 2002; McDonald & Augustine, 2020; McDonald & Mascagni, 2019; Pitkänen & Amaral, 1993; Vereczki et al, 2016). Although neuromodulatory (i.e., dopaminergic, noradrenergic, serotonergic, or cholinergic) inputs to the BNC also form symmetrical synapses, their main postsynaptic targets are distal dendrites and spines of PNs (McDonald, 2020).…”

Nonpyramidal neurons in the primate basolateral amygdala: A Golgi study in the baboon (Papio cynocephalus) and long‐tailed macaque (Macaca fascicularis)

“…Likewise, immunohistochemical studies of NPNs in the BNC of human and nonhuman primates have shown that subpopulations of these neurons express the calcium‐binding proteins PV (Pantazopoulos, Lange, Hassinger, & Berretta, ; Pitkänen & Amaral, ; Sorvari et al, ), CB (Pantazopoulos et al, ; Pitkänen & Amaral, ; Sorvari et al, ) and CR (McDonald, ; Sorvari et al, ), as well as the neuropeptides SOM (Amaral et al, ; Desjardins & Parent, ; McDonald et al, ; Schwartzberg, Unger, Weindl, & Lange, ), NPY (McDonald et al, ; Schwartzberg et al, ), and CCK (McDonald & Mascagni, ). The same morphological diversity of NPNs seen in the present Golgi study was also observed in the immunohistochemical studies of each of these calcium binding proteins and neuropeptides in primates.…”

“…There is evidence from light and electron microscopic studies in rodents and primates that different NPN subpopulations have different postsynaptic targets, and thus play specific roles in the circuitry of the BNC (McDonald, ). In both rodents (Bienvenu et al, ; Vereczki et al, ) and primates (Pitkänen & Amaral, ; Sorvari et al, ; McDonald & Mascagni, ), two separate GABAergic subpopulations, PV+ and CCK+ NPNs, are basket cells that innervate the soma and proximal dendrites of PNs. Remarkably, although a high density of pericellular baskets contacting PN somata are observed in the BNC in immunohistochemical studies of all species studied using antibodies to GABA, PV, or CCK, to the authors' knowledge they have not been described in Golgi studies of the BNC in any species, including the present study.…”