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Abstract

We analyzed the areal distribution of von Economo (VEN) and fork (FN) neurons in the human anterior insular cortex (AIC). The AIC, including the frontoinsula (FI), from eight freshly-fixed human brains (3 pairs of left and right insulae, and 5 single left or right insulae) were cut in the coronal plane at a 50-micron thickness. The sections were stained with cresyl violet to reveal all neuronal cell bodies and the proximal portion of their dendrites (Nissl stain), with silver nitrate to reveal myelinated fibers (Gallyas stain), or with an anti-parvalbumin antibody to reveal local interneurons. All stained sections were digitized with a 0.5-micron in plane resolution and 1-micron vertical stack using a scanning microscope. The distribution of the VEN and FN was charted using high-magnification examination of the Nissl slides. The AIC was parcellated using low-magnification examination of all three sets of slides with pre-established multi-architectonic criteria (Evrard et al., J Comp Neurol 2014 522:64-97). The VEN and FN were co-mingled within a rather vast region (or ‘VEN domain’) inside the ventral agranular region of AIC, with no apparent extension in the dorsal AIC or the dysgranular and granular insula. The VEN domain was delimited by a rather abrupt reduction of the numbers of both neurons. A comparison of the localization of the VEN domain with the architectonic parcellation of the AIC revealed (1) that its overall outer limit optimally overlapped with sharp architectonic boundaries, and (2) that it was further subdivided into at least three distinct architectonic areas (or ‘VEN areas’), rather than being homogeneous. While these three areas consistently occurred, their exact topology differed between the left and right hemispheres. Our prior examination of the macaque AIC revealed a complete overlap of the delimitation of a VEN/FN cluster with architectonic boundaries; however, this cluster formed one unique architectonic area, rather than being divided into several areas (Horn FM and Evrard HC, in preparation). The highly consistent overlap of the VEN distribution and architectonic boundaries (or “elemental localization”) in humans and monkeys indicates the existence of a robust selective pressure on the development of the AIC throughout evolution. The multiplication of the number of VEN areas likely correlates with the disproportionately faster growth of the AIC, including in particular FI, in humans compared to other primate species (Bauernfeind et al., J Hum Evol 2013 64:263-79). This multiplication might underlie the possible evolutionary emergence of the subjective awareness of feelings in the human AIC (Craig, Nat Rev Neurosci 2009 10:59-70).