Evolutionary specializations of primate brain systems

Abstract

Primates are distinguished from other mammals by a number of anatomical features, including convergent, close-set orbits; enlarged eyes; digits tipped with nails rather than claws; opposable hallux; and elongated calcaneus (Cartmill, 1992; Martin, 1990; Szalay et al., 1987). These shared, derived characters (synapomorphies) are generally thought to have arisen as adaptations in ancestral (stem) primates for nocturnal activity in the fine, terminal branches of trees (Martin, 1990). The behaviors that drove the evolution of primate anatomical synapomorphies remain at issue, with proposals including visually guided predation on insects and small vertebrates (Allman, 1977; Cartmill, 1972, 1974), foraging on fruits and flowers, in addition to predation (Rasmussen, 1990; Sussman, 1991), and a hindlimb-dominated " graspleaping" locomotor pattern (Szalay and Dagosto, 1988). If evolutionary history left its imprint on the primate body, what mark did it leave on the brain? Traditionally, studies of primate brain evolution have focused on changes in brain size and external morphology. Size and external morphology give little indication of evolutionary changes in internal brain organization, however, and, if modern neuroscience teaches us anything, it is that brains are internally structured and compartmentalized to an extraordinary degree. For example, mammalian cerebral cortex is comprised of several large histological domains (iso-, archi-, and paleocortex), each of which consists of multiple smaller divisions (cortical areas), which are composed of smaller, repeating units (modules), which are themselves composed of even smaller, vertically oriented neuronal clusters (minicolumns). Each of these structural compartments is composed of neurons that are connected to other neurons within the same compartment in very particular ways, and which are connected to the neurons of other cortical compartments in very particular ways. Far from being a diffuse neural net, as once was thought, mammalian cerebral cortex exhibits a degree of internal structural complexity unrivaled by any other biological tissue. Given such a view of the brain, it is easy to imagine how evolution might have modified its organization. One might expect, for example, that particular lineages evolved new compartments (areas or modules), or that ancestral mammalian compartments were reorganized internally in distinctive ways in different taxa, or that new systems of connections between compartments evolved in certain groups. In fact, many changes like these did occur during mammalian evolution (reviewed by Preuss, 2000, 2001). We face a considerable obstacle, however, in attempting to reconstruct the brain changes that accompanied primate origins-the paucity of comparative information. As a group, neuroscientists are inclined to concentrate their research on a few model animal taxa, under the assumption that the important features of mammalian brain organization are shared among mammals. In keeping with the modern biomedical research paradigm, neuroscientists have come to treat animals as standardized materials for exploring the organization of "the brain"-as though there were only one brain-rather than as resources for exploring the diversity of brains (Logan, 1999, 2001; Preuss, 2000; see also Raff, 1996). The result is while the brains of a select few taxa-especially rats and macaque monkeys-have been studied in great detail; much less effort has been devoted to other mammalian taxa. This places great limitations on our ability to reconstruct primate brain evolution. Fortunately, neuroscience has maintained a small cadre of investigators willing to buck the trend, maintaining an interest in evolution and a curiosity about differences in mammalian brain organization. A central figure in this group is Irving T. Diamond (see, for example, Diamond, 1973; Diamond and Hall, 1969). Diamond was greatly influenced by the writings of Elliot Smith and Le Gros Clark, and devoted himself to developing an evolutionary neuroscience of mammals. Moreover, he conveyed his enthusiasm for evolution to the very talented graduate students he attracted. Diamond, his students, and their associates have been responsible for a remarkable fraction of all the comparative studies of mammalian brain organization that have been published over the last 35 years. It is largely due to the efforts of these individuals that we know anything at all about the brains of strepsirhine primates, tree shrews, bats, and insectivores, and are therefore in a position to say something about the evolution of primate brain systems. This review is founded upon earlier works focusing on brain evolution at the level of structures and systems, particularly those of Allman (1977), Kaas (1980), Kaas and Preuss (1993), Pettigrew (1986; Pettigrew et al., 1989), Preuss (1993, 1995a), and Preuss and Kaas (1999). However, effort has been made to provide a more comprehensive and synthetic treatment of the subject of primate brain specializations than has previously been attempted. Many readers will, I fear, find the enumeration of neuroanatomical details rather too comprehensive for their liking. This degree of specificity is necessary, however, to illustrate the great number and variety of changes in brain organization that accompanied primate origins. Moreover, the very fact that neural changes were so numerous has important implications for students of behavioral evolution. © Springer Science+Business Media, LLC 2007.