Scientific Understanding of Consciousness
Evolution of Mammalian Brain
Science 20 May 2011: Vol. 332 no. 6032 pp. 955-957
Fossil Evidence on Origin of the Mammalian Brain
Timothy B. Rowe1, Thomas E. Macrini2, and Zhe-Xi Luo3
1Jackson School of Geosciences, University of Texas, C1100, Austin, TX 78712, USA.
2Department of Biological Sciences, St. Mary’s University, San Antonio, TX 78228, USA.
3Section of Vertebrate Paleontology, Carnegie Museum of Natural History, Pittsburgh, PA 15213, USA.
Many hypotheses have been postulated regarding the early evolution of the mammalian brain. Here, x-ray tomography of the Early Jurassic mammaliaforms Morganucodon and Hadrocodium sheds light on this history. We found that relative brain size expanded to mammalian levels, with enlarged olfactory bulbs, neocortex, olfactory (pyriform) cortex, and cerebellum, in two evolutionary pulses. The initial pulse was probably driven by increased resolution in olfaction and improvements in tactile sensitivity (from body hair) and neuromuscular coordination. A second pulse of olfactory enhancement then enlarged the brain to mammalian levels. The origin of crown Mammalia saw a third pulse of olfactory enhancement, with ossified ethmoid turbinals supporting an expansive olfactory epithelium in the nasal cavity, allowing full expression of a huge odorant receptor genome.
Brain size and sensory faculties diversified dramatically as mammals evolved to fill an immense variety of ecological niches, and much attention has been devoted to reconstructing the organization and origin of the ancestral mammalian brain. Among living taxa, mammals have the largest brains relative to body size and are unique in possessing the neocortex (isocortex). Accordingly, research has focused on origin of the neocortex and evolutionary increases in brain size [measured as a function of body mass].
Mammalia arose in or before the Early Jurassic [~200 million yeas ago (Ma)]. The oldest fossils are mostly tiny isolated jaws and teeth, and until now the rare skulls offered little detail on early brain evolution because internal access required destructive sampling. Comparative and developmental anatomy of living mammals has been our chief source of information. Such studies postulated numerous drivers for increased encephalization and origin of the neocortex, including innovations in hearing, feeding, taste, olfaction, miniaturization, parental care, endothermy, elevated metabolism, and nocturnality. Although deeply informative, few details have emerged on timing or sequences of historical events.
Here, we ask what sequence of evolutionary events culminated in the origin of the mammalian brain, and how was the brain in the ancestral mammal different from its closest extinct relatives? For this study, we used high-resolution x-ray computed tomography to nondestructively scan tiny fossil skulls of two basal mammaliaforms from the Early Jurassic of China.
The mammalian lineage (Synapsida) diverged from other tetrapods in the Carboniferous (~300 Ma). The braincase initially lacked fully ossified walls and floor; hence, little is known of early brain form. The first detailed view of the pre-mammalian brain is seen in basal Cynodontia, a clade originating in the Late Permian (~260 Ma) that includes living mammals and their proximate extinct relatives. The cynodont endocranial cavity is more fully enclosed. The olfactory bulbs were small, and the nose lacked ossified turbinals. The forebrain was narrow and featureless, the midbrain exposed dorsally, and the pineal eye persisted. The cerebellum was wider than the forebrain, and the spinal cord was narrow. The middle ear ossicles remained massive and attached to the lower jaw, and the cochlea occupied only a shallow bony recess. Compared with their living descendants, early cynodonts possessed low-resolution olfaction, poor vision, insensitive hearing, coarse tactile sensitivity, and unrefined motor coordination. Sensory-motor integration commanded little cerebral territory.
Morganucodon is the basal-most member of Mammaliaformes, a clade including mammals and their closest extinct relatives. It records a first major pulse in encephalization. The olfactory bulb and olfactory (pyriform) cortex are by far the regions of greatest expansion. A deep annular fissure encircles the olfactory tract, marking a distinctive external division of the mammalian brain between the olfactory bulb and cortex. The cortex is inflated and wider than the cerebellum, covering the midbrain and the pineal stalk. The cerebellum is also enlarged, implying expansion of the basal nuclei, thalamus, and medulla, and the spinal cord is thicker. The brain now resembles living mammals more than basal cynodonts in shape and proportions
Increased sensitivity in olfaction, and improved tactile resolution and motor coordination account for much of the first pulse in pre-mammalian encephalization. Enhanced high-frequency hearing is also implicated. The middle ear ossicles are highly reduced (but still attached to the lower jaw), and the cochlea is now prolonged into a short, curved tube. Comparative neuroanatomy suggests that neocortical expansion also supported an enhanced visual field, but bony correlates are lacking in these fossils.
Hadrocodium is the closest known extinct relative of crown Mammalia. It marks a second encephalization pulse. Expanded olfactory bulbs and olfactory cortex account for most of the increase. The middle ear ossicles are now detached from the jaw and suspended beneath the cranium, a condition otherwise confined to crown Mammalia. Growth of the olfactory cortex in early ontogeny of the living didelphid Monodelphis separates the auditory ossicles from their primary (and ancestral) attachment to the mandible to develop the same anatomical relations seen in Hadrocodium. This famous transformation evidently had little effect on hearing performance because the size and complexity of the cochlea is no different than in Morganucodon. The cerebellum in Hadrocodium bulges backward, bending the occipital plate into an arch that transmitted a thick spinal cord, implying enhanced motor-sensory integration.
The origin of crown Mammalia marks a third pulse of olfactory elaboration, as the ethmoid turbinals ossify to form both the cribriform plate and a rigid scaffold in the nasal cavity for epithelium containing the odorant receptor (OR) neurons. Activation of OR genes induces olfactory epithelial growth, in turn inducing turbinal growth and ossification. Ossified turbinals afford a 10-fold (or more) increase in olfactory epithelial surface within the nasal cavity. The maxilloturbinal also ossifies at this same time, affecting a sevenfold (or more) increase in respiratory epithelial surface. It functions in water balance, and its appearance in Mammalia ancestrally may reflect elevated metabolism.
Our data suggest that in basal mammaliaforms, a first pulse of encephalization was driven by increasing resolution in olfaction and tactile sensitivity and enhanced neuromuscular coordination. With a pelt, basal mammaliaforms were probably also endothermic, and the ontogeny of thermoregulation implies parental care. Endothermy may have been a consequence of encephalization because a large brain is metabolically expensive to maintain. However, metabolism is under hormonal regulation that does not command large cerebral regions, and thus did not itself drive encephalization. Hadrocodium records a second pulse of encephalization, probably also driven principally by olfaction.
The ancestral species of Mammalia amplified these inheritances in a third pulse of olfactory elaboration because its ossified ethmoid complex allowed full expression of its huge OR genome, which is an order of magnitude larger than in most other vertebrates. Only much later did acute visual and auditory systems evolve among mammals. In some descendents, the olfactory system was further elaborated, whereas in others it was reduced and supplanted by alternate sensory modalities, such as electroreception and sonar. But at its start, the brain in the ancestral mammal differed from even its closest extinct relatives specifically in its degree of high-resolution olfaction, as it exploited a world of information dominated to an unprecedented degree by odors and scents.
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