Chapter 7 - The insular cortex: A review

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Abstract

The human insular cortex forms a distinct, but entirely hidden lobe, situated in the depth of the Sylvian fissure. Here, we first review the recent literature on the connectivity and the functions of this structure. It appears that this small lobe, taking up less than 2% of the total cortical surface area, receives afferents from some sensory thalamic nuclei, is (mostly reciprocally) connected with the amygdala and with many limbic and association cortical areas, and is implicated in an astonishingly large number of widely different functions, ranging from pain perception and speech production to the processing of social emotions. Next, we embark on a long, adventurous journey through the voluminous literature on the structural organization of the insular cortex. This journey yielded the following take-home messages: (1) The meticulous, but mostly neglected publications of Rose, 1928, Brockhaus, 1940 are still invaluable for our understanding of the architecture of the mammalian insular cortex. (2) The relation of the insular cortex to the adjacent claustrum is neither ontogenetical nor functional, but purely topographical. (3) The insular cortex has passed through a spectacular progressive differentiation during hominoid evolution, but the assumption of Craig (2009) that the human anterior insula has no homologue in the rhesus monkey is untenable. (4) The concept of Mesulam and Mufson (1985), that the primate insula is essentially composed of three concentrically arranged zones, agranular, dysgranular, and granular, is presumably correct, but there is at present much confusion concerning the more detailed architecture of the anterior insular cortex. (5) The large spindle-shaped cells in the fifth layer of the insular cortex, currently known as von Economo neurons (VENs), are not only confined to large-brained mammals, such as whales, elephants, apes, and humans, but also occur in monkeys and prosimians, as well as in the pygmy hippopotamus, the Atlantic walrus, and Florida manatee. Finally, we point out that the human insula presents a unique opportunity for performing an in-depth comparative analysis of the relations between structure and function in a typical sensory and a typical cognitive cortical domain.

Introduction

The human insular cortex forms a distinct, but entirely hidden cerebral lobe, situated in the depth of the Sylvian fissure. The primordial insula is initially located on the free lateral surface of the cerebral hemisphere, but during further development, it lags behind and becomes gradually overgrown by adjacent regions of the hemispheres. As regards the structure of the insular cortex, Mesulam and Mufson, 1985, Mufson et al., 1997, Bonthius et al., 2005 recognized three concentrically arranged zones, a rostroventral agranular zone, a caudodorsal granular zone, and a wide, intermediate dysgranular (Ig) zone. The terms agranular and granular refer to the absence or presence of an internal granular layer (IV). The intermediate zone is termed dysgranular because granule cells are rather scarce in layer IV and do not display complete laminar differentiation. A special feature of the anterior insular cortex (AIC) is that its fifth layer contains, in addition to pyramidal neurons, numerous large spindle-shaped cells. Similar cells have been observed in the anterior cingulate cortex (ACC; von Economo, 1926). These distinctive elements, which have been termed: “von Economo neurons” (VENs; Allman et al., 2005, Ngowyang, 1932), have attracted much attention in the recent literature. It was initially believed that these cells are unique to humans and great apes (Allman et al., 2005, Nimchinsky et al., 1999), but it has been reported meanwhile that they also occur in whales (Hof and van der Gucht, 2007) and elephants (Hakeem et al., 2009). VENs are hypothesized to form part of circuits underlying decision making, complex social cognition, and self-awareness (Allman et al., 2005, Allman et al., 2010, Allman et al., 2011b, Allman et al., 2011a).

Section snippets

Neuroanatomical studies

Experimental neuroanatomical studies in monkeys, mostly rhesus macaques, summarized by Mesulam and Mufson, 1985, Mufson et al., 1997, Augustine, 1996, have shown that the insular cortex receives afferents from the dorsal thalamus and from several sensory cortical areas, is reciprocally connected with the amygdala as well as with several limbic and association cortical areas, and projects to the premotor cortex and the ventral striatum. Moreover, there is an abundance of local intrainsular

Functional studies

The insular cortex was long regarded simply as a viscerosensory and visceromotor region, based on the studies of Penfield and Rasmussen, 1950, Penfield and Faulk, 1955. These authors performed electrical stimulation of the insula during presurgical evaluations of a large number of temporal lobe epilepsy patients. During the past decades of the twentieth century, our insights into the functional significance of the insula rapidly progressed, enabling Augustine (1996) to list in an authoritative

Gross morphology of the human insula

The human insula or island of Reil forms a distinct cerebral lobe, which is buried in the depth of the sulcus lateralis. It is covered by adjacent parts of the frontal, parietal, and temporal lobes, known as the orbitofrontal, frontoparietal, and temporal opercula (Fig. 2a). The insula is shaped like a triangle, the apex of which is directed anterobasally. A deep sulcus circularis separates the insular lobe from the surrounding opercula. Owing to the triangular shape of the insula, separate

Presentation of data

Brodmann (1909) distinguished two cytoarchitectonic zones in the human insula, a granular posterior zone (J. post) and an AA zone (J. Ant). (The designation agranular indicates that an internal granular layer (IV) is entirely lacking.) The border between these two zones was found to correspond roughly, but not exactly to the central sulcus of the insula (Fig. 4a). Brodmann (1909, p. 146) states that it is difficult to divide the two insular zones into individual fields, and he adds that such a

Presentation of data

As the title of his classical work “Vergleichende Lokalisationslehre der Groszhirnrinde” indicates, Brodmann (1909) did not only confine himself to the cytoarchitecture of the human cortex but also included a number of other mammals in his analysis. The list of species studied by him includes a marsupial, the wallaby Macropus dorsalis; an insectivore, the hedgehog Erinaceus europaeus; a bat, the flying fox Pteropus rufus; a lagomorph, the rabbit Oryctolagus cuniculus; a rodent, the ground

Presentation of data

In a publication, mainly devoted to the acoustic cortex, Cajal (1900) pays brief attention to the insula. His description is based on Golgi-preparations of the insular cortex (no further specification) of a child of 1 month. This description is accompanied by an illustration, which is reproduced here in Fig. 11a. The capitals in bold used in what follows correspond to those in the figure. Cajal mentions that the fifth layer of the insular cortex contains, apart from numerous ordinary pyramids

The architecture of the human insular cortex: synopsis and perspective

All studies on the cytoarchitectecture of the human insular cortex carried out so far agree that this cortex contains a rostroventral agranular zone and a dorsocaudal granular zone. The agranular zone and its immediate surroundings are connected with limbic structures, such as the amygdala and the posterior orbitofrontal and anterior cingulate cortices. They are involved in the processing of autonomic and food-related information, and neuroimaging studies have shown that they are strongly

Acknowledgments

The author thanks Dr. Michel Hofman for asking him to contribute to this volume, and for not asking him to reduce the chapter to the limits originally set for it, Dr. Leonardo Cerliani for many, most stimulating discussions on “our” insula, Mr. Ton Put and Mr. Wil Maas for help with the illustrations, and to Suzanne Bakker M.Sc. for moral support and reference management. Finally, the author wants to acknowledge especially the invaluable and continuous assistance of Dr. Jenneke Kruisbrink, the

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