A volumetric comparison of the insular cortex and its subregions in primates

Abstract

The neuronal composition of the insula in primates displays a gradient, transitioning from granular neocortex in the posterior-dorsal insula to agranular neocortex in the anterior-ventral insula with an intermediate zone of dysgranularity. Additionally, apes and humans exhibit a distinctive subdomain in the agranular insula, the frontoinsular cortex (FI), defined by the presence of clusters of von Economo neurons (VENs). Studies in humans indicate that the ventral anterior insula, including agranular insular cortex and FI, is involved in social awareness, and that the posterodorsal insula, including granular and dysgranular cortices, produces an internal representation of the body’s homeostatic state.We examined the volumes of these cytoarchitectural areas of insular cortex in 30 primate species, including the volume of FI in apes and humans. Results indicate that the whole insula scales hyperallometrically (exponent=1.13) relative to total brain mass, and the agranular insula (including FI) scales against total brain mass with even greater positive allometry (exponent=1.23), providing a potential neural basis for enhancement of social cognition in association with increased brain size. The relative volumes of the subdivisions of the insular cortex, after controlling for total brain volume, are not correlated with species typical social group size. Although its size is predicted by primate-wide allometric scaling patterns, we found that the absolute volume of the left and right agranular insula and left FI are among the most differentially expanded of the human cerebral cortex compared to our closest living relative, the chimpanzee.

Figure 1

Phylogenetic tree of primates included in this study. The length of each branch represents the distance in evolutionary time. The number in parentheses represents the number of individuals of that species sampled.

Figure 2

Lateral views of insular cortex. In (A), the left insula of a human has been exposed by removing the overlying opercula. (B) and (C) are schematics displaying the cytoarchitecture of the insulae in Homo sapiens and Macaca mulatta, respectively. In both images, the insulae are parcellated into granular (Ig), dysgranular (Id), and agranular (Ia) regions. The relative positions of these subdivisions of insular cortex are similar in both species. The central sulcus of the insula (csi) is labeled in the human. Other notations: Anterior limiting sulcus (ALS); first (s1), second (s2), and third short gyri (s3); first (l1) and second long gyri (l2); inferior limiting sulcus (ILS); orbitofrontal operculum (ofo); frontoparietal operculum (fpo); temporal operculum (to); piriform olfactory cortex (poc); superior limiting sulcus (SLS). (A), (B), and (C) are modified from Nieuwenhuys (2012). All figures are oriented so the anterior surface is on the left. The figures are not to scale.

Figure 3

Nissl-stained coronal sections of insular cortex in (A) Homo sapiens and (B) Macaca maura. Human sections were taken from the online resources of the human brain Atlas at Michigan state University (https://www.msu.edu/~brains/brains/human/index.html). Macaque sections were photographed from the GAAP collection. The scale is the same for all sections within a species. The schematic at the top of the figure is a modified diagram of Macaca mulatta from Mesulam and Mufson (1982) to show the approximate anterior–posterior plane of each of the coronal sections, which are labeled by numbers. Arrows mark the transitions between cortical areas. The abbreviations are the same as in Figure 1. SLS and ILS refer to the superior and inferior limbs of the Sylvian fissure, respectively. In H. sapiens, FI is labeled. Other notations: caudomedial area of the auditory belt (CM), agranular insula (Ia), dysgranular insula (Id), granular insula (Ig), frontal opercular area (OPf), parainsular area (Pi), piriform olfactory cortex (POC), and ventral somatosensory area (VS). All images of a species share the scale indicated in the leftmost image.

Figure 4

Nissl-stained coronal sections of insular cortex in (A) Ateles geoffroyi and (B) Loris tardigradus. Sections from both species were photographed from the GAAP collection. The scale is the same for all sections within a species. The schematic at the top of the figure is a modified diagram of Macaca mulatta from Mesulam and Mufson (1982) to show the approximate anterior–posterior plane of each of the coronal sections, which are labeled with numbers. Arrows mark the transitions between cortical areas. The abbreviations are the same as those used in Figure 3. ‘SLS’ in the coronal series from the Loris refers to the bend in the cortical tissue that is homologous to the SLS. All images of a species share the scale indicated in the leftmost image.

Figure 5

Nissl-stained FI and VENs in the anterior insula of a human. The boxed region in A is magnified in B. C displays VENs under high magnification. FI is agranular insular cortex (A) that contains clusters of VENs in layer Vb. In humans and great apes, VENs (marked by arrows in B) are found in the highest density on or near the crowns of gyri. VENs are cells with a bipolar morphology (C). The cell in the lower left corner of C is a pyramidal neuron. Photomicrographs B and C are oriented with the pial surface at the top of the image.

Figure 6

Linear regressions of the total insula volume (A) and the volume of its subdivisions (B–E) in the left hemisphere against total brain volume. Results of both RMA (solid lines) and PGLS (dashed lines) analyses are shown. Because the VEN-containing portion of agranular insula in great apes and humans is referred to as FI in this study, agranular insula and FI are combined (6E) for agranular insula to be compared in all primate taxa included. Individual hominoid species are labeled with abbreviations of their scientific names (H. s. = Homo sapiens, Pa. t. = Pan troglodytes, Pa. p. = Pan paniscus, Po. p. = Pongo pygmaeus, Po. a. = Pongo abelii).

Figure 7

Asymmetry quotient (AQ) values for the insula as a whole and each of its cytoarchitectural subdivisions. Each specimen, in which volume estimates could be obtained for the left and right insulae and its cytoarchitectural subdivisions, is represented by its own symbol. Each symbol represents a single species. The whiskers extend to the largest/smallest observations within a distance of 1.5 times the interquartile range.