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The mammals first appeared in the fossil record approximately 190 million years ago, but did not radiate to fill a diverse variety of ecological niches until after the end of the Cretaceous period and the extinction of the dinosaurs. The lineage leading to mammals, including the therapsid and cynodont mammal-like reptiles, split off from the lineages leading to modern reptiles during the Carboniferous era, almost 300 million years ago. (Lambert et al., 1985). There are no living species which closely resemble these early mammal-like reptiles; thus, the evolutionary steps which presumably led from the reptilian brain to the mammalian brain are very difficult to trace.
Since the Paleocene radiation, a great diversity of mammalian species have arisen, exhibiting an equally great diversity of brain structure. However, all mammalian brains exhibit a number of features which are distinctive from those of any reptilian or amphibian brain. These differences extend even to the level of the medulla oblongata, where the diverse visceral and somatosensory inputs generally terminate in distinct nuclear structures which are linked by fascicular tracts to structures in the diencephalon and telencephalon. At the midbrain, the tectum is elaborated into the superior and inferior colliculi, and the hypothalamus is greatly elaborated. The differences are most evident in the cerebral hemispheres, where the relatively undifferentiated neuropil of the amphibians and reptiles is superseded by the highly specialized structures of mammalian neocortex and allocortex (limbic cortex.) The homologue of the reptilian dorsal ventricular ridge is not immediately evident in mammals; some authors have maintained that it is homologous to the mammalian amygdala (Carey, 1982; Johnston, 1915), while others argue that the cells of the dorsal ventricular ridge have migrated to become the source of the cells of the mammalian cortical plate (Deacon, 1990; Karten and Shimuzu, 1989; Mumford, 1994) and that the migration of the cells of the ependymal layer (at the ventricular surface) to the cortical plate during mammalian ontogeny may be a recapitulation of this evolutionary development.
MacLean's (1970) "triune brain hypothesis" is a broad, sweeping view of the history of vertebrate brain evolution. Maclean proposes that the primitive mammalian brain arose with the development of generalized cerebral cortex over the reptilian "R complex", and that the advanced mammals are distinguished by the further accretion of six-layered neocortex. While MacLean's view is helpful in some respects, it is also subject to a number of misinterpretations or over-interpretations. For example, the amphibian brain already includes precursors of mammalian limbic structures, and the reptilian brain includes areas in the primordial pallium which are homologous to mammalian neocortex, including their pattern of sensory projections to and from thalamic nuclei. Thus, the view that the characteristically mammalian structures were simply added to the brain late in evolution must be replaced by an interpretation in which the paleomammalian and neomammalian brains developed through a process of elaboration and differentiation from structures which already existed in the most primitive amphibian brain. Rather than thinking of the primate brain as a sort of layer cake, one might think of it as a balloon which has been stretched, more in the cortical areas than in the brain stem and limbic regions.
In the evolution of the mammalian brain from the reptilian and amphibian, very significant structural changes occur in the brain stem and mesencephalic regions as well as in the limbic system; that is, the "R system" is not strictly conserved in evolution. The exact functional significance of these changes is beyond the scope of this paper, but the idea that the mammalian brain contains within itself a complete and still-functioning reptilian core, appears to be an oversimplification.
Discussions of the "limbic lobe" as a functional unit (i.e. MacLean's "paleomammalian brain") should not obsure the fact that the limbic system consists of several structures with very distinctive evolutionary origins and cellular makeup. The pyriform cortex is possibly the least derived structure (most closely resembling its primordial origins) and is still involved with its original olfactory function. The hippocampus, by contrast, is a highly derived, multilayer structure (together with the dentate gyrus) which also exhibits an innovative biochemistry for long-term potentiation in mammals. Because of its connectivity, the cyngulate gyrus is considered part of the limbic system, but by cytoarchitectonic criteria, the cyngulate gyrus is fully developed six-layered neocortex.
Both the neocortex and the limbic system must be viewed as a major structural innovations of the mammalian brain. As MacLean noted, the structures of the limbic system have been largely conserved throughout mammalian evolution. However, it is also important to note that all species of mammals have significant areas of six-layered neocortex (as well as limbic cortex). While important differences exist between the cortex in different areas of the brain, and among mammalian species, nevertheless it is believed that the similarities outweigh the differences (Braitenberg and Schuz, 1991).
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