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Modular Subdivisions of Dolphin Insular Cortex: Does Evolutionary History Repeat Itself?

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Modular Subdivisions of Dolphin Insular Cortex: Does Evolutionary History Repeat Itself? Modular Subdivisions of Dolphin Insular Cortex: Does Evolutionary History Repeat Itself? Paul Manger, Monika Sum, and Michael Szymanski University of California, Davis Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/10/2/153/1758298/089892998562627.pdf by guest on 18 May 2021 Sam Ridgway Naval Command Control and Ocean Surveillance Center Leah Krubitzer University of California, Davis Downloaded from http://direct.mit.edu/jocn/article-pdf/10/2/153/1931754/089892998562627.pdf by guest on 30 September 2021 Abstract ■ The structural organization of the insular cortex in the cortex, varies dramatically. Indeed, despite the tremendous ex- bottlenose dolphin was investigated by examining Nissl- and pansion of the cetacean neocortex, the size of the modules in myelin-stained tissue that was sectioned coronally and tangen- the insular cortex is similar to that described for small-brained tially. An uneven distribution of cell clusters that coincided mammals like the mouse, suggesting that module size is evolu- with myelin-light zones was observed in layer II. When the tionarily stable across species. Selection for optimal-size proc- present observations were compared to descriptions of mod- essing units, in terms of the lengths of connections within and ules in other animals, we found that the range of module size between them, is a likely source of this stability. ■ is restricted, while the size of the brain, particularly the neo- INTRODUCTION Mountcastle (1978) was not a ªxed structure in the cortex, and he proposed that the cortex should “not be The notion that the neocortex is divided into functional regarded as a collection of isolated units cemented to- parts was popularized almost a century ago by Brod- gether in a mosaic.” mann (1909). Architectonic analysis of cerebral cortex in Recently, the term module has been used more vari- a variety of mammals led Brodmann to divide the neo- ably to refer to a number of conªgurations of horizontal cortex into separate ªelds, or areas. For decades the or tangential cell clusters that do not necessarily traverse belief that these cortical areas are the building blocks of all cortical layers, and even Mountcastle has proposed a processing networks has persisted. Investigators have modiªed rendition of his original thesis (1997). We attempted to subdivide the cortex into major functional deªne modules as small architectonic, neuroanatomical, parts and to construct intricate networks involving feed- and physiological territories that can be distinguished forward and feedback connections between cortical from other tissue within the classically deªned cortical ªelds (Kaas & Krubitzer, 1991; Van Essen, Anderson, & ªeld. These types of tangentially distributed modules Felleman, 1992). Others have striven to understand how within a cortical ªeld are exempliªed by the barrels of single neuron ªring patterns in sensory, association, and the primary somatosensory area of rodents (Woolsey & motor areas of the cortex interface with these global Van der Loos, 1970) and by the blobs of the primary networks and translate incoming sensory inputs into visual area of primates (Livingstone & Hubel, 1984). perceptions, cognition, memory, and learning. The Modules have been identiªed across species and difªculty of explaining psychological processes at a cel- across sensory systems (Krubitzer, 1995). Unlike cortical lular or cortical network level suggests that analysis at ªelds, they possess a uniformity in structure (Löwel, an intermediate level of organization may be necessary. Freeman, & Singer, 1987; Purves, Riddle, & LaMantia, Accumulating evidence indicates that within cortical 1992), interconnections (e.g. Livingstone & Hubel, 1984; ªelds, smaller units of construction are evident and are Krubitzer & Kaas, 1989), and neurophysiological proper- generally referred to as modules. Cortical columns or ties (Hubel & Wiesel, 1963; Livingstone & Hubel, 1984; modules were ªrst described by Mountcastle (1957) as Sur, Wall, & Kass, 1984; Ts’o, Frostig, Lieke, & Grinvald, an “elementary unit of organization of the somatic cor- 1990). They can be induced to form in development tex made up of a vertical group of cells extending (Constantine-Patton & Law, 1978), are susceptible, within through all cellular layers.” The module described by limits, to environmental inºuences (Hubel & Wiesel, © 1998 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 10:2, pp. 153–166 1970; Durham & Woolsey, 1984; Löwel & Singer, 1992), Microscopic and macroscopic examination of the are computationally predictable (Mitchison, 1991), and stained frontal sections revealed four architectonic sub- may better explain cortical evolution than the cortical divisions of the dolphin anterior insular cortex. The pres- ªeld (Krubitzer, 1995). These structures contribute to the ent study concerns the largest and most distinct of these larger organization of functional divisions called cortical architectonic ªelds, Ia, which has an area of approxi- ªelds. Their ubiquity throughout the mammalian cortex mately 900 mm2 (60 mm mediolateral, 15 mm anteropos- leads us to question not only their function but also their terior). Within Ia, an irregular clumping of cells in layer evolutionary signiªcance. II was observed (Figures 2A and 3).1 This clumping was One way to address these questions is from a com- markedly different from the laminar patterns observed parative perspective. By examining a variety of species in other regions of the insula (Figure 2B). The cell clus- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/10/2/153/1758298/089892998562627.pdf by guest on 18 May 2021 we can ascertain similar features of organization, due to ters in layer II ranged in size from 125 to 450 µm in common ancestry (homology), and modiªcations in or- diameter and had a mean diameter of 255 µm. The ganization related to species specialization. More impor- prominent cells within the layer II clusters were verti- tant, examining the products of the evolutionary process cally oriented pyramidal cells, with somas approximately Downloaded from http://direct.mit.edu/jocn/article-pdf/10/2/153/1931754/089892998562627.pdf by guest on 30 September 2021 will allow us to understand how the mechanisms that 10 to 12 µm wide. However, smaller cells were abundant generate change, which are governed by ontogenetic in these clusters, the staining techniques used did not constraints, interact with selective pressures to shape allow us to assign a particular classiªcation to these the brain organization of extant mammals. remaining cells. Although not explicitly described, a simi- The goal of this study is to examine an animal that has lar clumping of cells can be observed in a previous study a large neocortex that evolved independently from that of the cytoarchitecture of the insular cortex of the dol- of humans in an effort to determine if large brains are phin (Jacobs et al., 1984). constructed in a similar fashion, independent of recent Myelin stains of adjacent cortical sections also demon- evolutionary history. The speciªc question we can begin strated an irregular staining. When the adjacent myelin to answer regarding animals with big brains, particularly and Nissl sections were aligned using blood vessels as a humans, is how do the constraints imposed on nervous guide, it was found that the myelin-dense regions sur- system construction affect cortical processing strategies rounded the cell clusters (Figure 4). Layer I of the region and in turn the complex neural and morphological spe- examined showed dense myelin staining. Within layer II, cializations associated with our species. cortical ªbers were seen to form fascicles that passed between the clumps of cells observed in Nissl-stained sections. Where there were cell-dense clumps, there was METHODS AND RESULTS a distinct lack of staining for myelin. Fibers from layer I In the present investigation, the entire brains of two were observed to form bundles that passed through bottlenose dolphins (Tursiops truncatus) were removed layer II and became less distinct in layer III. Fibers from and ªxed, postmortem, in 10% formalin for approxi- these bundles could be seen to enter the regions where mately 2 years. These brains were cut into 1-cm slabs in the layer II cell clusters were located (Figure 4B). Por- either a frontal or a sagittal plane. From these slabs, the tions of the ªber bundles that passed through layer II region of cortex termed the insula (Morgane & Jacobs, appeared to be made up of ªbers coming from deeper 1972) was dissected free from the remainder of the brain cortical layers. slab (Figure 1). The particular region investigated his- In order to get an appreciation of the geometric ar- tologically was located at the anterior portion of the rangement of cell clusters and myelin-dense regions, the insula and termed the anterior insular area, or Ia (Jacobs, cortex sectioned tangential to the pial surface was simi- Galaburda, McFarland, & Morgane, 1984). This area was larly stained and examined. The extreme gyriªcation of found to overlay the claustrum, as does the insula in the dolphin cortex and the prolonged ªxation of the primates. In the dolphin, however, this portion of cortex tissue prevented a manual ºattening of the cortical sheet, surrounds the lateral edge of the thalamus and the infe- as has been achieved in other mammals (Krubitzer, rior portion of the basal ganglia, which resides just ven- Clarey, Tweedale, Elston, & Calford, 1995). Some portions tral
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