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date: 08 December 2019

Evolution of Neocortex for Sensory Processing

Summary and Keywords

The neocortex is a part of the forebrain of mammals that is an innovation of mammal-like “reptilian” synapsid ancestors of early mammals. This neocortex emerged from a small region of dorsal cortex that was present in earlier ancestors and is still found in the forebrain of present-day reptiles. Instead of the thick structure of six layers of cells (five layers) and fibers (one layer) of neocortex of mammals, the dorsal cortex was characterized by a single layer of pyramidal neurons and a scattering of small, largely inhibitory neurons. In reptiles, the dorsal cortex is dominated by visual inputs, with outputs that relate to behavior and memory. The thicker neocortex of six layers in early mammals was already divided into a number of functionally specialized zones called cortical areas that were predominantly sensory in function, while relating to important aspects of motor behavior via subcortical projections. These early sensorimotor areas became modified in various ways as different branches of the mammalian radiation evolved, and neocortex often increased in size and the number of cortical areas, likely by the process of specializations within areas that subdivided areas. At least some areas, perhaps most, subdivided in another way by evolving two or more alternating types of small regions of different functional specializations, now referred to as cortical modules or columns. The specializations within and across cortical areas included those in the sizes of neurons and the extents of their processes, the dendrites and axons, and thus connections with other neurons. As a result, the neocortex of present-day mammals varies greatly within and across phylogenetically related groups (clades), while retaining basic features of organization from early ancestral mammals. In a number of present-day (extant) mammals, brains are relatively small and have little neocortex, with few areas and little structural differentiation, thus resembling early mammals. Other small mammals with little neocortex have specialized some part via selective enlargement and structural modifications to promote certain sensory abilities. Other mammals have a neocortex that is moderately to greatly expanded, with more cortical areas directly related to sensory processing and cognition and memory. The human brain is extreme in this way by having more neocortex in proportion to the rest of the brain, more cortical neurons, and likely more cortical areas.

Keywords: cortical areas, columns, visual cortex, motor cortex, neurons

Introduction

While the neocortex is a critical part of the brain in mammals, it is not a new part, as the name implies. Instead, aspects of neocortical organization can be traced back at least as far as the early amniotes, those vertebrates that evolved egg-covering membranes that allowed their eggs to develop on land as an important adaptation to reproduction on land. These amniotes produced two major lines of evolution, the reptilian-like synapsids that led to a varied radiation, with only one surviving branch, modern mammals. The other line, the sauropsids, produced the living members of the reptilian radiation, including birds (e.g., Bininda-Emonds & Hartmann, 2017). Mammal-like synapsids and early mammals were varied, but most died out, leaving the small surviving line of monotreme mammals that separated some 220 million years ago from the line that led to the only somewhat more successful marsupial radiation that separated from the highly diverse line of placental mammals 140–215 million years ago (Bi et al., 2018; Rowe, 2017). Placental mammals are represented by four major superorders: the Afrotheria ranging from elephants to golden moles; the Xenanthra of sloths, armadillos, and anteaters; the Euarchontoglires of rodents, tree shrews, and primates; and the highly varied Laurasiatheria of shrews, bats, carnivores, ungulates, and whales (Murphy et al., 2004). Roughly 5,400 species of mammals now exist.

The synapsid ancestors of early mammals had a region of the forebrain that was likely very much like the dorsal cortex of present-day reptiles such as turtles. In reptiles, dorsal cortex is sensory and dominated by visual inputs relayed from the retina via the dorsal lateral geniculate nucleus in the thalamus, as this nucleus relays to the primary visual cortex in mammals. Another source of visual input to the dorsal cortex in reptiles is via the projection from the retina to the optic tectum of the midbrain (called the superior colliculus in mammals) where visual information is relayed to the visual thalamus and then to dorsal cortex. This pathway exists in modern mammals as a projection from the superior colliculus to part of the visual thalamus (part of the inferior pulvinar, also called the lateral posterior nucleus), which relays to visual cortex in the temporal cortex (Baldwin et al., 2017). The ancestors of early mammals and reptiles likely had somatosensory inputs and auditory inputs processed subcortically (Medina, 2007). Thus, early mammals inherited from amniotic ancestors a region of the dorsal cortex that was predominantly visual, with two sources of visual input. Overall, the processing was rather simple (Shepherd, 2011; Fournier, Muller, & Laurent, 2015), with the summation of sensory inputs in dorsal cortex and outputs to hippocampal cortex and subcortical motor centers (Kaas, 2017a).

The major change in sensory processing that occurred with the emergence of early mammals was the evolution of the six-layered neocortex from the single layer of neurons in dorsal cortex, with auditory and somatosensory as well as visual inputs from the thalamus all terminating on small neocortex neurons, the stellate neurons, that defined the middle layer of neocortex, layer 4. Instead of summing sensory inputs from an array of thalamic neurons, so that their individual contributions were lost, layer 4 neurons preserved most of the sensory information from individual thalamic neurons, such as when and where the skin was touched or where an object was in visual space. This preserved information was then distributed and used in various ways in the cortex. This change in sensory processing was critically important as it provoked the evolution of serial and higher-order sensory processing at the cortical level and the emergence of secondary and higher-order visual, auditory, and somatosensory areas that received preprocessed sensory information from primary and other sensory areas. Thus, the major sensory inputs were to layer 4 where neurons preserved sensory information so that it could be processed further in layer 3 for distribution to other newly evolved sensory areas, while layers 5 and 6 provided sensorimotor information to subcortical stations and sensory feedback to cortical areas and thalamic nuclei.

Given the evolution of neocortex from the dorsal cortex and the potential that the neocortex had for further often species- or clade-specific modifications, some of the major ways that the sensory cortex evolved in mammals can be considered. It is useful to start with a brief description of how the neocortex of early mammals was subdivided into functionally distinct areas, as deduced from comparative studies of cortical organization in mammals, and then proceed to examples of the types of changes evident in various present-day mammals.

The Organization of Neocortex in Early Mammals

Evolution of Neocortex for Sensory ProcessingClick to view larger

Figure 1. A lateral view of a reconstructed brain of an early mammal. The olfactory bulb and olfactory (piriform) cortex made up much of the brain of the small, nocturnal mammals. Neocortex was a smaller part of the forebrain as a cap on olfactory cortex. Primary somatosensory (S1), visual (V1), and auditory (A1) areas as shown. Other visual areas include prostriata, the second visual area, V2, and a temporal visual area, T. S1 is bordered by a rostral (RS) and a caudal (CS) somatosensory area, and the second somatosensory area, S2, is lateral to S1. Gustatory (g) on taste cortex is ventral to S1. Frontal cortex is divided in sensory-related medial frontal (MF) and orbital frontal (OF) areas. The medial wall of neocortex of each hemisphere is not visible but is folded out in the diagram to show cingulate cortex, CC, and retrosplenial cortex, RS. The superior colliculus, SC, and the larger inferior colliculus, IC, make up the upper half of the midbrain.

Current concepts of how the neocortex was organized in early mammals are based on what is called a cladistic analysis, and it is constrained by knowledge from the fossil record on the shape and size of brains of early mammals (Kaas, 2017a). Overall, the fossil record indicates that early mammals were mainly small, mouse to rat sized, and had small brains with proportionately little neocortex (Rowe, 2017). In favorable fossils, the brain size and shape closely correspond to the internal surface of the skull, and casts of the inside of the skull indicate the shape and size of the brain. The shallow rhinal fissure along the lateral surface of the brain marks the transition of the more dorsal neocortex to the more ventral piriform or olfactory cortex, and this fissure is sometimes apparent in the endocasts of the skull. Thus, it is known that the neocortex was only a small cap on the much larger olfactory cortex of the forebrain. The cladistic approach of inferring ancestral states rests on the assumption that features or traits that are widely present across members of the clade were likely present in the common ancestor. Thus, across mammals, evidence exists for the presence of a primary visual area (V1), auditory area (A1), and somatosensory area (S1) in similar locations in neocortex (Figure 1). The presence of other areas is a bit uncertain, but it can be concluded that visual cortex included at least four visual areas, and somatosensory cortex had four or five. Other areas are those indicated in Figure 1. Note that there was no primary motor area or premotor areas, as these areas did not appear until the evolution of placental mammals (Kaas, 2017a).

In early mammals, olfaction was clearly the most dominant sense judging from the proportion of the forebrain occupied by olfactory cortex. Primary somatosensory cortex was large, and much of the lateral two thirds of the representation responded to the facial whiskers, the nose and lips, and the tongue and teeth. Narrow somatosensory areas bordered S1 rostrally and caudally, and a second area, S2, was lateral to S1. Early mammals had sensory guard hairs as well as underfur (Rowe, 2017). Visual cortex was less important for the nocturnal mammals, as the primary visual area, V1, was rather small. However, V1 was bordered medially by a visual-limbic area, prostriata, that guided behavior. A second visual area, V2, was located along the lateral cortex of V1, as in present-day mammals. And a temporal visual area, T, received information about moving objects, such as prey and predators, from relay from the superior colliculus to the pulvinar to cortex. Taste was evaluated subcortically in a small region of taste cortex and, together with olfactory information, in orbital-frontal cortex. With few areas, many behavioral functions, such as motor control and simple responses to stimuli, largely depended on subcortical brain structures.

Sensory Specialization of Neocortex in Mammals with Selective Expansions of Sensory Cortex

One common form of evolutionary change has been to selectively expand one of the primary sensory areas in neocortex over the others or selectively expand some parts of sensory representations over others (Krubitzer & Kaas, 2005). The converse of this evolutionary change has been to selectively reduce a representation when its functions are not fully needed. A notable example of the selective expansion of visual cortex is the primary visual cortex (V1) of a small nocturnal primate, the tarsiers that are found in Southeast Asia. At 21% of neocortex or more (estimates sum as high as 50%, but 21% seems more accurate), proportionately more neocortex is devoted to V1 than any other mammal (Collins et al., 2005; Wong et al., 2010). V1 is not only larger but has cortical layers and sublayers that are more structurally differentiated and specialized than in other mammals. Tarsiers also have very large eyes in comparison with their body, head, and brain. The large eye provides a light-gathering advantage in dim light, and the large size of V1 allows the details of the visual scene to be well represented. This improved vision would be important in the evolution of tarsiers as they became nocturnal and acquired their unique behavioral specializations of being such an extreme visual predator of insects and small vertebrates that they ate no vegetable food. Primary visual cortex V1, in this primate, became the main processer of visual information. Other mammals with a relatively large V1, such as tree shrews (Wong & Kaas, 2009) and squirrels (Wong & Kaas, 2008), also have a greatly enlarged part of the visual midbrain, the superior colliculus, which is also enlarged (the optic tectum) in highly visual birds.

In contrast to such highly visual mammals, the blind mole rat has practically no V1, and the small remnant that remains may not even have visual functions (Cooper et al., 1993). Such a reduced visual cortex is clearly an adaptive response to their dark underground environment where object vision was not possible. Yet, they receive enough light to regulate circadian and reproductive behavior via retinal projections to subcortical structures.

For an emphasis on the somatosensory system, the duck-billed platypus, an egg-laying monotreme from Australia, appears to have proportionately the most neocortex devoted to primary somatosensory cortex, where much of S1 represents their highly sensitive “bill.” In addition to touch, the bill is also sensitive to weak electric fields, such as those given off by muscle contractions of underwater prey. Thus, S1 has electroreceptive and tactile functions (Krubitzer et al., 1995; Krubitzer, 1996). As the platypus hunts its prey in murky waters, it closes its eyes and ears, so it is fully dependent on S1 and other somatosensory areas. The large amount of somatosensory cortex and the corresponding small amounts of visual and auditory cortex are consistent with its behavior. As another example, raccoons have a greatly enlarged representation of their sensitive hands in S1, and they are extremely proficient in searching for prey in the water with their hands (Welker & Seidenstein, 1959). As a third example, the specialized receptor surface of the star-like nose of the star-nosed mole has a large representation in somatosensory cortex (Catania, 2011). In addition, naked mole rats, which use their teeth extensively to dig tunnels and carry objects, have a very large cortical representation to their front teeth (Catania & Remple, 2002). And bats especially represent their touch receptors on wings that are used to guide flight (Calford, Graydon, Huerta, Kaas, & Pettigrew, 1985; Marshall et al., 2015; Sterbing-D’Angelo et al., 2011). However, as somatosensory processing is important to all mammals, mammals with little or no somatosensory cortex should not be expected to be found, although those mammals protected with a hard shell, as in armadillos, or sharp quills, as in hedgehogs, may have less somatosensory cortex, but if so, the difference from what may be expected is not great (Kaas, 2011b).

When considering auditory cortex, echo-locating bats have a neocortex that is dominated by auditory cortex, including a very large A1 with an expanded representation of the biosonar pulse frequency (Covey, 2005; see Kaas, 2011b for a comparative review). In contrast, the auditory system and the auditory cortex may be selectively small in mammals that spend nearly all of their lives underground where locating auditory stimuli is less complex and sounds from outside are less important. While primary somatosensory cortex occupies much of neocortex in naked mole rats, the primary auditory cortex, defined histologically, appears to be very small (Catania & Remple, 2002). Hearing behaviors in mole rats are limited, and major brainstem auditory nuclei are relatively small (Heffner & Heffner, 1993).

Convergent Evolution of Visual Cortex in Highly Visual Tree Shrews and Squirrels

Although squirrels are Rodentia and tree shrews are Scandentia, branches of the Euarchontoglire superorder that separated perhaps 80 million years ago, they look enough alike for tree shrews to be mistaken as species of squirrels. In addition, their visual systems, and especially visual cortex, are very similar. Both have large eyes with retinas dominated by cones for detailed vision, and both have an expanded visual system. In particular, both have a large portion of neocortex that is devoted to primary visual cortex and have six to seven similar visual areas. In primary visual cortex, V1, there are some differences. Squirrels and tree shrews do not have the layer 3 “blobs,” a specialization for perceiving color that characterizes V1 of all primates, suggesting that this feature evolved in early primates or their immediate ancestors (Kaas, 2012). As a closer relative of primates than rodents, tree shrews have the stimulus orientation selective modules in V1 that are found in all primates, while squirrels and other rodents do not (Van Hooser, 2007). Thus, this feature of V1 likely evolved before the divergence of the tree shrew branch from the primate branch (Kaas, 2017c).

Tree shrews and squirrels also have a well-developed second visual area, V2. In both mammals, V2 has a similar series of six to seven modular subdivisions. Lateral to V2, there are band-like subdivisions that resemble V3 of primates. More ventrally, caudal areas of the temporal cortex receive a relay of inputs from the superior colliculus via the caudal pulvinar (Wong et al., 2008; Baldwin, Balaram, & Kaas, 2017). This temporal area in tree shrews and squirrels resembles the middle temporal visual area MT of primates, but unlike MT, these temporal areas do not get inputs from V1. This is an old pathway to temporal cortex in mammals that has been expanded in tree shrews and squirrels as they both adapted to a diurnal lifestyle by emphasizing detailed vision to detect predators and feeding opportunities at a distance.

The Evolution of an Extended Cortical Visual System in Primates with a Dorsal Stream for Visual–Motor Actions and a Ventral Stream for Object Identification

Primates are unusual in that they clearly vary in numbers of areas of cortex. Prosimian galagos have about 50 cortical areas per cerebral hemisphere, smaller New World monkeys (marmosets) have about 80, macaque monkeys 140, and humans perhaps 200 (Kaas, 2017c). The number of visual areas also appears to be variable across primate taxa, while being greater in all primates than in most mammals. While absolute numbers are hard to determine and visual areas may be multisensory or visual-motor, raising issues of identification, an early estimate of the number of visual areas in macaque monkeys was 32 (Felleman & Van Essen, 1991). Now, a few more visual areas could be added to that number, and humans would have even more. The evolution of such complex cortical networks is poorly understood, but the result is that much more information is derived from the retinal inputs and used to guide and choose behaviors. Similar, but less complex cortical networks exist in the auditory and somatosensory systems of primates. Here, the focus is on the visual cortex, its main features of organization, and how one visual area, the middle temporal visual area, may have evolved.

All or nearly all mammals have “two visual systems” (Schneider, 1969). One of these two systems depends on the better-known retina to lateral geniculate nucleus to primary visual cortex pathway, which distributes visual information to other areas of cortex. This system is better suited for identifying predators, food, and other objects of interest. The other system is the retina to superior colliculus to pulvinar to temporal cortex pathway, and this system is better suited to detecting changes in the visual environment, such as the movement of a predator, and providing information on what to do, and then guiding that action. As the visual functions of the two streams overlap, lesioning V1 to inactivate one system, or the superior colliculus to inactivate the other, produced major changes in visual behavior, but considerable visual function remained. With the evolution of primates, something changed to make the V1 distribution system more dominant. Thus, humans with V1 lesions have so little remaining vision that the remaining visual behaviors are called “blind sight” (Stoerig & Cowey, 1997).

In primates, primary visual cortex projects to a new target in the center of the territory in temporal cortex that is activated in other mammals by the superior colliculus to pulvinar to cortex pathway. This target in temporal cortex of primates is known as the middle temporal visual area, MT (Allman & Kaas, 1971). As a result, MT directly, or indirectly through V2 and V3, gets activating input from V1 and provides a good part of the distribution of visual input to the “vision for action” cortical system. Areas immediately around MT (MTc, F5Td, FSTv, MST) still receive inputs from the superior colliculus via the pulvinar, but they are also functionally tied to V1 through connections with each other and MT (Kaas & Morel, 1993). MT and these four areas project to targets in a greatly expanded posterior parietal cortex, where visual information is directly or indirectly provided to a series of action-specific “domains” in a more anterior part of the posterior parietal cortex. These domains in turn project to functionally matched domains in motor and premotor cortex where motor actions are initiated (Kaas & Stepniewska, 2016). This cortical sequence of processing to produce actions has been called the dorsal stream of visual cortical processing in primates (e.g., Ungerleider & Haxby, 1994). As this dorsal pathway provides information about changes in the visual environment and the relationships of the locations of objects in the environment, it is called the “where” pathway. However, the dorsal pathway also provides information about what to do and how to do it, known as the “how” pathway (Goodale & Milner, 1992). As part of the dorsal stream, the posterior parietal domains have an important role in the selection of the appropriate visually guided action (thus, in decision making). The non-primate ancestors of early primates did not have this elaboration of visual processing steps in a dorsal stream, the elaboration of posterior parietal cortex including action-specific domains for further sensory planning, and action-specific elaboration of motor and premotor cortex to have sequences of functionally matched domains. Likewise, the ventral stream, specialized for object identification and perception, has been elaborated by adding a number of areas and domains in the inferior temporal lobe for the identification of individual faces and classes of objects (Rolls, 2003). Of course, these two streams interact at several levels, as perception is an important aspect of action selection.

Taste Cortex

The parts of the cortex representing taste have not been as extensively studied across a range of mammalian species as have the visual, auditory, and somatosensory cortical areas. Yet, the comparative evidence suggests that early mammals had a small region of taste cortex just lateral to somatosensory cortex representing touch on the teeth and tongue and next to the more ventral rhinal fissure (Figure 1). This is the region where taste is represented in well-studied rats and mice and in many other studied mammals. In mice, different populations of neurons in primary taste cortex are responsive to bitter, sour, salty, umami, or sweet-tasting substances (Chen et al., 2011), and this mapping of taste classes is likely mapped in a similar way in primary taste cortex of other mammals. Orbital-frontal cortex is often considered a secondary level of processing taste in a multisensory region in mammals (Rolls, 2006). Comparative studies of cortex responsive to taste substances have been too limited to reveal much on how this cortex has evolved to reflect the food specializations of different mammals. However, species differences in taste receptors and taste behavior have been more widely studied (e.g., Glaser et al., 1995; Nofre, Tinti, & Glaser, 1996). Thus, there is no sensitivity to sweet, and therefore no cortical representations of sweet in at least some mammals that eat mainly flesh, (e.g., cats) or blood (vampire bats) (Jiang et al., 2012). Pandas, in contrast, which feed mainly on bamboo, lack a functional umami receptor, so this flavor would not be represented in cortex. Other mammals, sea lions and dolphins, swallow their fish prey whole, so they have little use of taste in selecting or rejecting food. As a result, their taste systems are greatly atrophied. Major variations in primary taste cortex likely reflect the loss of the representation of one or more of the taste categories as taste receptors that are not needed become dysfunctional due to reduced selection. Other mammals that eat many different kinds of food need to identify and remember those foods that are safe to eat and those that are beneficial. Thus, the information from taste receptors is very important, and it becomes even more useful when it is combined with olfactory and visual information in orbital-frontal cortex (Rolls, 2006). The connections between primary taste cortex and orbital-frontal cortex are widespread in primates (Kaas et al., 2006), reflecting the importance of higher-order processing of taste information with information from other sensory systems.

Olfaction

Olfaction, or smell, is mediated by two main divisions of the olfactory system, the main olfactory subsystem and the accessory olfactory subsystem. Both subsystems were well developed in early mammals, as judged by the fossil endocasts of the skulls (Rowe, 2017). Such skulls, when well preserved, indicate that early mammals had large olfactory bulbs and a large expanse of piriform or olfactory cortex that was greater than all of neocortex (Figure 1). For the main olfactory system, projections from olfactory receptors terminate in the olfactory bulb. The olfactory bulb sends projections to piriform cortex, which has as many as four distinct regions or “areas,” and to the amygdala. Both the amygdala and piriform cortex project to part of the thalamus, which provides one of the inputs to orbital-frontal cortex. The accessory olfactory system starts with a specialized receptor surface, the vomeronasal organ, accessed via the roof of the mouth, and the receptor cells project to the accessory olfactory bulb, which then projects to subdivisions of piriform cortex and the amygdala, which relay to the thalamus and to orbital-frontal cortex. A large olfactory system was very important to early mammals, as they were nocturnal and small and needed to detect distant food, mates, and predators, recognize offspring and other relatives, and define home territories. While some mammals have retained a well-developed olfactory system, other mammals have reduced or lost parts of the system. The two olfactory subsystems functionally overlap somewhat, but the main olfactory subsystem, with most of about 1,000 receptor types, is concerned with a broad range of environmental smells as they relate to food and predator detection (Mori et al., 1999), while the accessory olfactory subsystem is concerned with a much smaller number of receptors that respond to pheromones for social-sexual signaling, including the regulation of emotions and mating behavior (Keverne, 1999). The olfactory system, including olfactory cortex, has commonly regressed in aquatic mammals where the uses of olfaction are limited. Genes for receptor types have become nonfunctional as their functions were no longer needed, and the representations of these receptors in olfactory cortex were lost. In monotremes, the olfactory bulb is small in the aquatic platypus but remains large in the echidna, which detects food at a distance on land (Ashwell, 2013). Whales have lost their olfactory system. For other reasons, some primates have lost much of their olfaction. Present-day primates are divided into three large groups or clades: Strepsirrhine or prosimian galagos, lemurs, and lorises; Platyrrhine (New World) monkeys; and Catarrhine (Old World) monkeys, apes, and humans. The Strepsirrhine primates have well-developed main and accessory olfactory systems, and scent marking of territories is important to them. Most of these primates are nocturnal where olfaction is usually important. New World monkeys have proportionately less olfactory cortex, but good olfactory systems. They are diurnal except for one nocturnal monkey. Catarrhine primates are diurnal and have proportionately less olfaction cortex and a greatly reduced or nonfunctional accessory olfactory system (Bhatnarger & Smith, 2007). In humans, the accessory olfactory system is nonfunctional. These reductions and losses are thought to reflect the greater dependence on vision in diurnal primates with extremely well-developed visual systems. More specifically, the common ancestors of Catarrhine primates had evolved trichromatic color vision, and this was used to evaluate sociosexual cues. Thus, the need for pheromonal communication was reduced or eliminated (Gilad et al., 2004).

Conclusions

In this article, ways in which sensory cortex evolved from the organization in early mammals to present-day mammals are discussed. Early mammals were small and had only a small cap of neocortex on the rest of the forebrain. This small amount of neocortex included about 20 functionally distinct regions, the cortical areas. These were primary visual, somatosensory, and auditory areas, as well as three or four additional visual areas, at least three more somatosensory areas, and likely at least one higher-order auditory area. Taste was represented in primary taste cortex and again in multisensory orbital-frontal cortex. The olfactory bulbs and primary olfactory (piriform) cortex were large, as olfaction was very important in these small, nocturnal mammals. As mammals evolved in different ways to occupy a range of different environments, visual, somatosensory, and auditory neocortex became generally more important and olfaction became less important, so sensory areas in neocortex often expanded and increased in number. In primates with a fovea, this small part of the retina became overrepresented in cortical visual areas, allowing for detailed vision. A major line of primate vision evolved trichromatic vision and a large number of visual areas. As vision dominated behavior in these primates, including humans, olfaction became less critical, and the accessory olfactory system was lost. In general, mammals had several representations of the skin of the opposite side of the body in the neocortex of each cerebral hemisphere, with an emphasis on representing the longer sensory hairs on the face and a few other locations on the body. These long sensory hairs have provided contact information about objects while they were short distances from the body. Also, the tongue, teeth, lips, and glabrous nose were important surfaces that had enlarged representations in cortical somatosensory areas, while the glabrous skin of the hands dominated much of these representations in most primates. A few New World monkeys had large cortical representations of their prehensile tail, which functioned like a hand. Raccoons independently evolved large cortical representations of the glabrous stem of their hands. All mammals needed somatosensory representations, but a few had only crude representation of most of the body other than the face and limbs. Early mammals were nocturnal and had evolved high-frequency hearing. Thus, they could communicate in the dark at frequencies that reptilian predators could not hear. Auditory cortex remains important in present-day primates, and especially in humans where auditory communication is so critical. Thus, primates have two to three primary auditory areas, as many as eight secondary areas, and additional third-level areas. Echolocating bats evolved to have greatly enlarged parts of auditory areas of cortex that represent the very high frequencies that are used in echolocation of prey and objects in dim light. They also evolved special hair receptor types on the wings to help guide flight (Sterbing-D’Angelo et al., 2011). In some mammals specializing in certain foods, the taste cortex lost representations of taste substances that were not part of their diet, such that sugar and sweet were not represented in the cortex of some mammals that only ate meat, or a meat flavor was not represented in pandas that ate bamboo. Mammals that returned to fully live in water lost olfaction, and those that ate fish whole had reduced taste systems. Finally, mammals specialized sensory areas at the modular level in several ways. Primates have divided primary visual cortex into “blob-like” regions spaced over V1 for processing color information, and other regions with orderly arrangements of orientation-selective neurons in columns for object detection, as well as direction of motion detection. The close relatives of primates do not have blobs in V1, and only a very close relative, the tree shrew, also has the orderly arrangement of orientation-specific columns in V1. Thus, as the branches of mammalian evolution diversified, sensory areas of cortex changed their internal organizations, including the addition of modular structures, sensory areas enlarged or decreased in size and sometimes greatly increased in numbers of sensory areas, and thus the steps and kinds of sensory-perceptual processing. In addition, especially in primates, the numbers of sensory-motor areas increased for guiding and controlling motor behaviors and deciding on what actions best suited the sensory circumstances.

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