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Abstract:
We recently demonstrated the presence of the large spindle-shaped von Economo neuron (VEN) in a specific architectonic area (‘VEN-area’) in the anterior insula in the macaque monkey (Evrard et al., Neuron, 2012, 74:482-9). Given its relatively large size and localization in layer 5a, the VEN likely projects to distant brain regions including the midbrain periaqueductal gray (PAG). A prior tracing study demonstrated that distinct areas in the macaque anterior insula project densely to PAG (An et al., J Comp Neurol, 1998, 401:455-79). Here, using previously published (An et al., 1998) and new material, we examined (1) the distribution of neurons retrogradely labeled in the insula with injections of cholera toxin b, fast blue or fluorescent dextran in different columns of PAG, (2) whether any of the architectonic areas projecting to PAG corresponds to the VEN-area, and (3) whether the VEN and its co-mingled companion ‘fork’ cell (FC) project to PAG. Injections in PAG invariably labeled small, discontinuous patches of neurons in the ventral portion of the insula both posterior and anterior to the limen insula. Using a recently refined architectonic map of the macaque insula (Evrard et al., J Comp Neurol, 2014, 522:64-97), we observed that the areal affiliation of these patches consistently varied with the location of the injection site. Injections in the dorsal lateral column of PAG (dlPAG) sparsely labeled the fundal agranular area (Ivfa), and the dorsal and ventral posterior agranular areas (Iapd and Iapv), posterior to the limen, and densely labeled the intermediate agranular area (Iai), anterior to the limen, as reported before by An et al. (1998). Injections in the lateral column of PAG (lPAG) labeled the ‘mound’ dysgranular area (Idm) and the dorsal posterior agranular area (Iapd), posterior to the limen, and the lateral agranular insula (Ial), anterior to the limen. Injections in the ventrolateral column of PAG (vlPAG) produced an intermediate labeling including both Iai and Ial. VENs and fork cells were located preferentially, if not exclusively, in Ial. An analysis of the morphology of the neurons retrogradely labeled in Ial revealed a small subset of VENs and fork cells. The projection of directly adjacent insular areas to different columns of PAG may provide a unique insight in the efferent cortical control of the autonomous system. In this context, the VEN and their companion FC could have a direct and rapid influence on the sympathetic and parasympathetic substrate of emotional behavior and feelings.
