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WIREs Cogn Sci
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The evolution of brains from early mammals to humans

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Abstract The large size and complex organization of the human brain makes it unique among primate brains. In particular, the neocortex constitutes about 80% of the brain, and this cortex is subdivided into a large number of functionally specialized regions, the cortical areas. Such a brain mediates accomplishments and abilities unmatched by any other species. How did such a brain evolve? Answers come from comparative studies of the brains of present‐day mammals and other vertebrates in conjunction with information about brain sizes and shapes from the fossil record, studies of brain development, and principles derived from studies of scaling and optimal design. Early mammals were small, with small brains, an emphasis on olfaction, and little neocortex. Neocortex was transformed from the single layer of output pyramidal neurons of the dorsal cortex of earlier ancestors to the six layers of all present‐day mammals. This small cap of neocortex was divided into 20–25 cortical areas, including primary and some of the secondary sensory areas that characterize neocortex in nearly all mammals today. Early placental mammals had a corpus callosum connecting the neocortex of the two hemispheres, a primary motor area, M1, and perhaps one or more premotor areas. One line of evolution, Euarchontoglires, led to present‐day primates, tree shrews, flying lemurs, rodents, and rabbits. Early primates evolved from small‐brained, nocturnal, insect‐eating mammals with an expanded region of temporal visual cortex. These early nocturnal primates were adapted to the fine branch niche of the tropical rainforest by having an even more expanded visual system that mediated visually guided reaching and grasping of insects, small vertebrates, and fruits. Neocortex was greatly expanded and included an array of cortical areas that characterize neocortex of all living primates. Specializations of the visual system included new visual areas that contributed to a dorsal stream of visuomotor processing in a greatly enlarged region of posterior parietal cortex and an expanded motor system and the addition of a ventral premotor area. Higher visual areas in a large temporal lobe facilitated object recognition, and frontal cortex included granular prefrontal cortex. Auditory cortex included the primary and secondary auditory areas that characterize prosimian and anthropoid primates today. As anthropoids emerged as diurnal primates, the visual system specialized for detailed foveal vision. Other adaptations included an expansion of prefrontal cortex and insular cortex. The human and chimpanzee–bonobo lineages diverged some 6–8 million years ago with brains that were about one third the size of modern humans. Over the last 2 million years, the brains of our more recent ancestors increased greatly in size, especially in the prefrontal, posterior parietal, lateral temporal, and insular regions. Specialization of the two cerebral hemispheres for related, but different functions became pronounced, and language and other impressive cognitive abilities emerged. WIREs Cogn Sci 2013, 4:33–45. doi: 10.1002/wcs.1206 This article is categorized under: Neuroscience > Anatomy

Early mammal brain. The proposed organization of the neocortex of early mammals. This reconstruction was based on a cladistic analysis of common features of neocortex of present‐day mammals, and information about brain size and proportions inferred from endocasts of the skulls of early mammals. Primary somatosensory cortex, S1, was bordered by a rostral somatosensory area, SR, a caudal somatosensory area, SC, and a ventral secondary area, S2. A ventral gustatory area, g, may have been present as part of an ‘insula’ region near the rhinal sulcus, a shallow dimple in early mammals. Perirhinal and postrhinal areas were likely present. Auditory cortex (aud) had at least one primary area, and perhaps secondary areas, while visual cortex included a primary area, V1, the second area, V2, a temporal visual area, T, and a medial prostriata visual area. Cortex of the medial wall of the cerebral hemisphere included granular (RSg) and agranular, RSa, retrosplenial areas, and dorsal (ccd) and ventral (ccv) cingulate cortical areas. The frontal cortex included orbital frontal, OF, and medial frontal, MF, areas. A large hippocampus, connecting with entorhinal cortex, folded under caudal and medial neocortex. Piriform (olfactory) cortex was proportionately large, and the olfactory tract and bulb are shown. The small cap of neocortex failed to cover the midbrain, and the superior colliculus, SC, and inferior colliculus, IC, were exposed.

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Owl monkey cortex. The organization of neocortex in a New World owl monkey. Nearly all of the cortical areas shown here are those shared by all primates. Macaque monkeys, apes, and humans have larger brains with more cortical areas. Compared to early mammals, primates have an array of visual areas, including V1, V2, and V3, rostral and caudal dorsolateral areas, DLr and DLc, a dorsomedial area, DM, a medial area, M, a prostriatal area, PS, a middle temporal area, MT, and associated areas, MTc, MST, FSTd, and FSTv, and perhaps four subdivisions of inferior temporal cortex, IT. Anterior parietal cortex includes a primate area, 3b or S1, bordering areas 3a and 1 (compare with SR and SC of early mammals) and an area 2. Somatosensory areas of the lateral sulcus (LS) include S2, the parietal ventral area, PV, and rostral and caudal divisions of ventral somatosensory cortex, VSr and VSc. Primary auditory cortex includes A1, the rostral area, R, and the rostrotemporal area, RT. A belt of secondary auditory areas includes the caudomedial area, CM. The parabelt represents a third level of cortical auditory processing. Motor cortex includes the primary area, M1, dorsal and ventral premotor areas, PMD and PMV, a supplementary motor area, SMA, with a eye (E) movement region, a frontal eye field, FEF, adjoined by a frontal visual area, FV, and rostral and caudal cingulate motor areas, CMAr and CMAc. The insular cortex has a gustatory field in the region of the parietal rostral, PR, cortex. Posterior parietal cortex, PPC, contains a more rostral half divided into domains for specific movements, PPC move, and a caudal half dominated by visual inputs. As for all eutherian mammals, there is a corpus callosum, cc. Only part of the hippocampus, Hip, is shown where it adjoins postrhinal cortex.

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