The origin and evolution of neocortex: From early mammals to modern humans

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The origin and evolution of neocortex: From early mammals to modern humans

3 Jon H. Kaas*

Department of Psychology, Vanderbilt University, Nashville, TN, United States *Corresponding author: Tel.: 1-615-322-6029; Fax: 1-615-343-8449, e-mail address: [email protected]

Abstract Human neocortex evolved in a series of ancestors with less neocortex and fewer cortical areas. Thus, early mammals had little neocortex and roughly 20 cortical areas, while early primates had much more cortex and around 50 cortical areas. Humans have the largest of primate brains that is 80% neocortex with about 200 areas. Other changes include more and more complex cortical networks, such as those for language, and modular and cellular specializations within areas. These and other changes allow the impressive mental abilities of humans.

Keywords Neocortex, Primates, Apes, Humans, Cortical areas, Language

1 Introduction Humans are unique in that they have extensive knowledge of the beliefs, morals, customs, music and art of their culture (Boyd, 2018). They have learned how to get food and otherwise maintain life. They recognize hundreds to thousands of other people, and know something about them. They acquired a complex language, and perhaps more than one. They have the complex knowledge essential to their occupations, and the math skills related to one’s work and play. They have vast knowledge about foods and how to prepare them. They rapidly consider vast amounts of information in order to select actions. Variations in cultural knowledge and skills have allowed our species to occupy even the extremes of this earth. All this and more is possible because of the human brain, which is the largest primate brain, of which 80% by volume is neocortex. Although the neocortex interacts extensively with other parts of Progress in Brain Research, Volume 250, ISSN 0079-6123, https://doi.org/10.1016/bs.pbr.2019.03.017 © 2019 Elsevier B.V. All rights reserved.

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the brain, none of these human abilities are possible without neocortex. Thus, understanding the organization of the human brain and especially neocortex is an important goal. Much of our present understanding has come from direct studies of human brains, especially recently with the aid of functional imaging. However, a deeper and perhaps different understanding can emerge through efforts to describe the evolution of human brains from those of distant ancestors with simpler brains. In addition, there is much to gain from studies on how brains, including human brains, develop. Human brains are not the largest, but they have the most neurons in neocortex (HerculanoHouzel, 2016), and in cortical organization, they might be the most complex. However, our brains are costly to maintain and few species could bear the cost of the 20 years or more it takes for a human brain to fully mature. Here the focus is on neocortex because it is such a critical part of the human brain. We start with a review of what the first mammals were like, and consider how their neocortex was most likely organized, based on comparative studies. Next, we consider the probable organization of the immediate ancestors of early primates, followed with early primates, early monkeys, apes, the hominid ancestors of humans, and modern humans. This journey is similar to a reversal of “The Ancestor’s Tale” from recent to ever more distant ancestors by Dawkins (2004). Here we consider simpler to more complex brains of present day vertebrates that resemble distant-to-recent ancestors. Of course, present day species are not ancestors, but they allow inferences to be made about ancestors (Kaas, 2017).

2 The origin of neocortex All mammals have some neocortex, but it varies considerably in size and organization across mammalian taxa. Reptiles have a dorsal cortex and birds have a Wulst, both parts of the forebrain that are considered homologous to the neocortex of mammals (Striedter, 2005). About 340 million years ago, some amphibians evolved the ability to lay and hatch eggs on land by protecting them from drying out with an outer membrane, the amnion. The early amniotes branched into two major radiations, the sauropsids that led to present day reptiles and birds, and the synapsids that led to mammals, but no other surviving branch. The dorsal cortex of reptiles, and especially turtles, is a simple structure that likely resembles an early precursor to neocortex in the reptile-like early synapsids (Fournier et al., 2015; Shepherd and Rowe, 2017). Turtles have a forebrain with a large olfactory bulb projecting to lateral cortex, the clear homolog of piriform cortex in mammals, a small cap of dorsal cortex, the homolog of neocortex, and medial cortex, the homolog of the hippocampus of mammals. These three divisions of cortex resemble each other in having a central cell layer of mainly pyramidal neurons capped by a layer of input axons connecting with apical dendrites, and a deep layer of output axons. There are a few subpial interneurons and middle layer 2 stellate interneurons, some of which may be inhibitory. The inputs to dorsal cortex are from the thalamus, and the outputs are to the

2 The origin of neocortex

hippocampus and to subcortical structures. Much of the dorsal cortex of turtles gets visual input from the dorsal lateral geniculate nucleus of the thalamus (Hall and Ebner, 1970), as does primary visual cortex of mammals. Lesions of dorsal cortex in turtles impair the habituation of protective responses (head withdrawal) to an approaching object (Killackey et al., 1972). There appears to be no auditory input to dorsal cortex. The existence of somatosensory input to the rostral part of dorsal cortex has been suggested (Kaas and Preuss, 2014), and there is somatosensory input to the Wulst in birds (Medina and Reiner, 2000). Accepting that the early synapsid ancestors of mammals had a dorsal cortex much like present day turtles (Molnar, 2011), the questions that remain are (1) how did the single layer of pyramidal neurons evolve into five layers of neurons in early neocortex; and (2) how did a predominantly visual dorsal cortex acquire somatosensory, auditory, and other thalamic inputs? The answers to those two questions remain uncertain, at least in regard to details. A thicker cortex of five cell layers likely resulted from more cell divisions from precursor cells that migrate from the ventricular zone to the surface of the forebrain to form a series of radial units or columns, and the enlargement of cortex would result from an earlier division of precursor cells to form more radial glia and thus more radial units (Rakic, 1988, 1995). Comparative studies of cortical development in mammals provide further insight. For example, marsupials and placental mammals diverged from each other over 100 million years ago, and some marsupials (opossums) have fewer neurons per unit of cortical surface in all cortical layers, and a shorter period of neuron generation than placental mammals (e.g., Cheung et al., 2010). This difference suggests that there are several regulatory mechanisms that control the numbers of cell divisions in precursor cells, and that other mammals, especially large brained primates, have evolved the advantage of more densely packed cortical neurons at the cost of longer developmental times. The other unknown is how the newly emerging layered neocortex acquired new inputs. Many of these inputs, most notably auditory and somatosensory inputs from the medial geniculate nucleus and the ventroposterior nucleus of the thalamus, project to another brain structure in reptiles and birds, the dorsal ventricular ridge. This structure is likely homologous to the claustro-amygdalar complex of mammals (Striedter, 2005). Axons from the thalamus that terminated in the dorsal ventricular ridge of early amniotes continued to do so in reptiles and birds, and the sizes and functions of the dorsal ventricular ridge expanded. In proto-mammals, these thalamic projections also involved the expanding neocortex, and this target became the dominant structure for sensorimotor processing and cognition (Striedter, 2005). While this interpretation of results remains in dispute (e.g., Briscoe and Ragsdale, 2018), the accumulating evidence supports the view that neocortex evolved from dorsal cortex via a process of enlargement by the radial and tangential addition of many more neurons (Molnar et al., 2014). Comparative studies of the subdivisions of neocortex of mammals indicate the number of cortical areas varies greatly, but a small number of cortical areas, about 20, are consistently found across members of the three major branches of mammalian

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evolution (Kaas, 2011a,b). These areas include primary and secondary visual, somatosensory, and auditory areas, as well as prefrontal, cingulate, retrosplenial and pararhinal areas, and likely a primary area for taste. All placental mammals also have primary and secondary motor areas, but these are not found in marsupials, and were most likely not present in early mammals. Cortical influences on motor behavior were likely limited, and largely dependent on somatosensory cortex, including a rostral somatosensory area for proprioception. The arrangement of cortical areas is best reconstructed from those mammals with small brains and little neocortex, thus suggesting further resemblance to the brains of early mammals. Quite remarkably, the cortical areas in American opossums (Beck et al., 1996; Catania et al., 2000; Wong and Kaas, 2009) and Australian possums (Elston and Manger, 1999; Huffman et al., 1999) are highly similar, even though these two lines of marsupial evolution have been independent for over 150 million years (Nilsson et al., 2010). Such mammals with little obvious change in body form and brain organization over millions of years are most informative in efforts to reconstruct the probable organization of the brains of early mammals. It remains uncertain as to how a primitive neocortex, with little histological differentiation between areas, acquired as many as 20 cortical areas from a distant ancestor with a dorsal cortex of perhaps only visual input. And the mechanisms for the increase in cortical areas to as many as 200 or more per hemisphere in the human brain are even less understood. For now, the relative positions of primary sensory areas depend on the graded expression of regulatory genes in the developing neocortex (e.g., Armentano et al., 2007; Grove and Fukuchi-Shimogori, 2003).The duplication and subsequent differentiation of areas is one possible way of increasing the numbers of cortical areas (Allman and Kaas, 1974). Or areas may be subdivided by new inputs that create modules that become new areas (Krubitzer and Hunt, 2007). For those cortical areas with major thalamus inputs, the arealization of cortex is thought to depend on chemo-affinity of afferents for specific regions of cortex (see Super and Uylings, 2001).

3 Early mammals Early mammals were small and largely nocturnal. The nocturnal environment was safer from the large diurnal dinosaurs that co-existed with early mammals until these reptiles were wiped out by the large meteorite that struck the earth 65 million years ago with worldwide consequences. Early mammals adapted to the safer nocturnal environment by having a coat of hair and a metabolic rate that maintained a functional body temperature. As they were nocturnal, early mammals were less dependent on vision, the sensorimotor functions of the superior colliculus were reduced, and the emerging neocortex became more important (Diamond and Hall, 1969; Heesy and Hall, 2010). In contrast, the optic tectum, the homolog of the superior colliculus, remained a highly important sensorimotor structure in reptiles and birds. The presence of long, sensory guard hairs on the face and other key parts of the body of early mammals (Rowe, 2017) allowed objects to be detected and appreciated at a short but useful distance from the body, and their somatosensory

3 Early mammals

information was processed in primary and secondary representations in neocortex. Auditory information became more important due to the nocturnal habitat. Size reductions and other changes in the bones from the mandible that came to form the middle ear (Luo et al., 2007), and the increased length of the cochlea, extended hearing into higher frequencies, permitting communication signals between parents and offspring that would be undetected by reptilian predators (Allman, 1999). Auditory inputs reached cortex, and were processed by one or more auditory areas (Kaas, 2011a,b). Taste was processed in taste cortex, and with olfactory and other sensory inputs in orbital-frontal cortex (Rowe and Shepherd, 2016). Other features that emerged with or just before early mammals include an increase in types of olfactory receptors and receptor genes, more sensory representation of the mouth and teeth at cortical levels and improved motor control with and sensory guidance from muscle spindle receptors. Relative to body size, early mammals had somewhat larger brains with larger cerebral hemispheres than their mammal-like ancestors (Rowe, 2017). The proportionately large olfactory bulb and cortex, as documented in the fossil record, indicate that olfaction was very important (Fig. 1).

FIG. 1 The proposed organization of neocortex in early mammals. The small size of the brain and the small cap of neocortex compared to olfactory bulb and cortex reflects evidence from fossil skull endocasts that indicate that the small early mammals had small brains with little neocortex. The proposed number of cortical areas, about 20 and not all shown, and their locations are based on comparative studies of extant mammals. Visual areas included primary (V1) and secondary (V2) areas, a temporal area (T), and prostriata on the medial wall of the hemisphere. Somatosensory areas included primary (S1) and secondary (S2), and rostral (RS) and caudal (CS) somatosensory areas. Auditory cortex (AUD) was mainly a primary field (A1). Posterior parietal cortex (PPC) was small, and mainly visual. Frontal cortex included medial frontal (MF) and orbital frontal (OF) divisions. A small gustatory area (g) probably existed. Medial wall cortex included cingulate and retrosplenial areas. The midbrain superior colliculus (SC) and inferior colliculus (IC) were not covered by neocortex. See Kaas and Preuss (2014) for details.

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4 Early primates and other archontoglires Early primates are part of a larger radiation of mammals, the euarchontoglires that include rodents, lagomorphs, scandentians (tree shrews) and dermoptera (flying lemurs). Formerly, the Supraorder Archontoglire included bats, but they are now in another Supraorder, Laurasiatheria (Murphy et al., 2004). Tree shrews and flying lemurs are most closely related to primates, but little is known about cortical organization in flying lemurs. However, tree shrews, as for primates, have expanded occipital and temporal regions of cortex that are devoted to vision, with a number of visual areas that somewhat resemble those in primates (Kaas, 2002). In addition, primary visual cortex has a modular organization with groups of neurons selective for specific stimulus orientations, as in primates (Fitzpatrick, 1996). Rodents formed a highly varied and successful radiation of 2300 or more species, with some rodents, squirrels, resembling tree shrews in having a large amount of cortex devoted to vision, and an arrangement of visual areas that are primate-like (Negwer et al., 2017; Van Hooser and Nelson, 2006). Squirrels and tree shrews also have a large region of temporal cortex that receives visual information from the superior colliculus via a relay from the pulvinar of the visual thalamus, as do primates (Baldwin et al., 2017a,b). These areas contribute to a primitive “dorsal stream” of visual processing. Thus, features of visual cortex expansion and organization may have evolved in the archontoglire ancestors of primates. The fossil record reveals features of the cortical evolution of brain size (Kaas, 2017). The now extinct relatives of early primates, the adapvids, omomyoids and plesiadaptiforms had brains with somewhat less neocortex than that of early primates (Rowe, 2017; Silcox et al., 2010). Extant primates also constitute a highly varied order of mammals (Fleagle and Seiffert, 2017). There are over 500 recognized species of living primates and perhaps more. The time of origin for the order is still somewhat uncertain, but molecular estimates push back this time to 70–90 million years ago (Murphy et al., 2004). Primates have been divided into two major groups or clades. One branch, the strepsirrhines or “wet-nosed” primates, includes lemurs, galagos and lorises, which are generally more primitive than members of the other branch of haplorhines or drynosed primates (Kay et al., 1997). The haplorhine primates include an early surviving branch, the tarsiers (formerly included with strepsirrhines as prosimians) and the other anthropoid primates that gave rise to New and Old World monkeys (Kay, 2015). Old World monkeys led to apes, and apes to humans. Early primates were small, nocturnal and adapted to the “fine-branch niche” (Martin, 1990; Ross and Martin, 2007). Their grasping hands and feet, small size, and forward facing, large eyes, allowed them to hold on to thin, bending branches in bushes and trees to grasp insects and other small prey, as well as fruits and buds (Bloch and Boyer, 2002). The neocortex was enlarged in proportion to the rest of the forebrain, and the larger temporal and occipital regions of the neocortex indicated a greater investment in the cortical processing of visual information. Eye-handcoordination would have been important as food objects were grasped and carried to the mouth. As the eyes were large, and the snout reduced, bringing living prey

4 Early primates and other archontoglires

to the mouth compared to grasping with the mouth likely reduced the risk of eye damage. Overall, the organization and functions of neocortex would have been largely like the smaller strepsirrhine primates, especially the mouse lemurs (Saraf et al., 2019), but also much like the somewhat larger but more studied brains of the African galagos (Wong and Kaas, 2010). While there have been few studies of their brains, mouse lemurs are of interest to those concerned with the evolution of primates because they are the smallest of primates at 50–90 g, and have the smallest of primate brains (2.5 g). They are thought to resemble the earliest of primates (Le Gros Clark, 1931), who were also small (Gebo, 2004). Lemur species evolved in Madagascar from a single ancestral species that was small like present-day mouse lemurs, and had somehow rafted from Africa some 60–70 million years ago. Now mouse lemurs are the most widespread and abundant of the Madagascar lemurs. Their small cerebral hemispheres are remarkably primate-like in overall shape, with a large temporal lobe extending ventrally and forward. The lateral fissure is the only visible fissure, with a calcarine fissure indenting visual cortex from the medial wall of each hemisphere. Architectonically, a number of sensory and motor areas have been identified (Saraf et al., 2019), including primary visual cortex, V1 or area 17. As in all other primates, area 17 has a modular organization reflecting the cytochrome oxidase (CO) “blobs” that mark axon terminations in layer 3 of axons from the koniocellular layers of the dorsal lateral geniculate nucleus (Casagrande and Kaas, 1994). Such “blobs” characterize V1 in all studied primates but not in any non-primate relatives in the archontoglire clade. Much of V1 is bordered by V2, and there is evidence for a V3. The middle temporal visual area, MT, stands out as a very distinct visual area in a number of histological preparations, as in other primates. More rostrally, near the upper end of the lateral fissure, cortex with clear sensory features, appears to be the primary auditory area, A1, perhaps together with the rostral auditory area, R. More rostrally, in frontal cortex, the primary somatosensory field, area 3b or S1, is easily identified, with a presumptive thin area 3b along its rostral border. Primary motor cortex, with agranular features, was identified just rostral to area 3b. Overall, these sensory and motor areas highly resemble those of the more extensively studied galago cortex in relative position and shape. African galagos are another strepsirrhine primate that offer a more extensive view of how the neocortex of early primates was likely organized. Architectonic, anatomical, microelectrode recording, and micro-stimulation studies on galagos have identified a number of cortical areas that also have been identified by these methods in New and Old World monkeys, suggesting that the 50 or so proposed areas in galagos (Wong and Kaas, 2010) were present in the common ancestors of strepsirrhine primates and monkeys. These include visual areas V1, V2, V3, V4 or DL, DM, prostriata, MT, MTc, MST, FST, and subdivisions of the visually responsive temporal lobe. Auditory cortex includes the primary area A1, the rostral primary area R, and likely an auditory “belt” of several secondary fields. Somatosensory cortex includes S1 (area 3b), area 3a, a presumptive area 1, the second somatosensory area, S2, and the parietal ventral area, PV. Motor areas include primary motor cortex (M1),

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dorsal (PMd) and ventral (PMv) premotor areas, the frontal eye field (FEF), and the supplementary motor area (SMA). Frontal cortex includes granular frontal cortex, a division thought to be specific to primates (Preuss and Goldman-Rakic, 1991), orbital frontal cortex, and medial frontal cortex. Cingulate cortex includes cingulate motor and sensory areas, and retrosplenial cortex includes granular and agranular areas. Additionally, perirhinal cortex includes taste cortex, as well as other areas. Many uncertainties remain because cortical areas can be difficult to identify, and most have not been identified by multiple criteria. But the main point is that there are a large number of cortical areas, on the order of 50 or so, and roughly two–three times as many as in early mammals; and these areas fall into the “primate pattern” that has been revealed in New and Old World monkeys (Zhu and Vanduffel, 2019). The proposed arrangement of some of the areas and regions of neocortex of an early primate, as reconstructed from shared features of strepsirrhine primate brains, are shown in Fig. 2. Before moving on to anthropoid primates, there are a few more features of neocortex of galagos that are important to mention. The first concerns posterior parietal cortex (PPC). Only a small mediolateral strip of cortex can be reasonably defined as posterior parietal cortex in rodents and tree shrews, while primates have a large posterior parietal region (Kaas et al., 2018). This cortex in galagos includes a medial portion that appears to have sensory-limbic functions. The larger part of posterior parietal cortex on the dorsal surface of the cerebral hemisphere is divided into a caudal part that is dominated by inputs from more caudal visual areas, and a rostral part with less direct visual inputs and many connections with higher order somatosensory cortical areas, as well as direct projections to premotor and motor cortex. Most importantly, rostral PPC is divided into eight or more subregions or domains where electrical stimulation produces different complex movements such as aggressive or defensive movements of the face, eye movements, reaching, grasping, moving the hand to the mouth, defense of head with the arm, and running or climbing in a lateral to medial sequence of domains. Nothing quite like this occurs in rodents or tree shrews, and other non-primates, although some movements can be evoked from the narrow PPC of tree shrews (Baldwin et al., 2017a,b). Each domain in PPC projects to functionally matched domains in premotor and primary motor cortex, where highly similar movements can be evoked by electrical stimulation (Kaas and Stepniewska, 2016). Importantly, a similar arrangement of posterior parietal cortex, premotor and motor cortex domains have been described in New World monkeys, and to a lesser extent, in Old World macaque monkeys. These are suggestive evidence that such an arrangement of domains exists in humans, with additions occurring with tool use and language production (see Kaas et al., 2018). Overall, all primates appear to differ from non-primate relatives by devoting large regions of parietal and frontal cortex to selecting specific responses based on sensory inputs, learning, memories and motivations. Galagos share a number of motor and premotor areas with other primates, suggesting that these areas were present in early primates (Wu et al., 2000).

4 Early primates and other archontoglires

FIG. 2 Proposed areas of neocortex in an early primate. These primates were shaped very much like those of small, present-day strepsirrhine primates. The relative enlargements of occipital, temporal, and posterior parietal regions reflect the importance of the processing of visual stimuli in all primates, and the presence of granular frontal cortex (c Fe) and the MT complex of the middle temporal visual area (MT) and the associated fundal superior temporal area (FST). The medial superior temporal area (MST) and the MT crescent (MTc) are all primate innovations. Other areas and regions include visual areas V1, V2, and V3, the dorsomedial visual area (DM) and the dorsolateral visual area (DL or V4). The inferior temporal caudal and rostral regions (ITc, ITr) are visual and have subdivisions, while the superior temporal regions (ST) have bimodal visual and auditory functions. Primary auditory cortex (Aud) includes A1 and probably the rostral auditory area (R). An auditory belt (A. belt) of several secondary areas surrounds the primary areas. Posterior parietal cortex includes two large divisions, a caudal region (PPCc) that is visual, and a rostral region (PPCr) that is sensorimotor, with functional subdivisions for specific actions (Domains). Anterior parietal cortex contains three somatosensory fields, the primary tactile area, S1 or Area 3b, the proprioceptive area, 3a, and a caudal strip of cortex, area 1–2 that is divided into areas 1 and 2 in many anthropoid primates. In addition to primary motor cortex (M1), frontal cortex has dorsal and ventral premotor areas (PMD and PMV), a supplementary motor area (SMA) and a frontal eye field (FEF). Orbital frontal cortex (OFC) is an important frontal region. Other areas are on the medial wall of the cerebral hemisphere, as on the banks of the deep central fissure. Note the olfactory bulb remains prominent, and these early primates had a highly functional accessory olfactory system.

A related specialization of primate brains is a major modification of the two cortical visual systems of non-primate mammals (Schneider, 1969). Non-primate relatives of primates have two sources of visual input to cortex; one by the well-known retina-to-dorsal lateral geniculate to V1 pathway, and the other by a

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lesser known retina-to-superior colliculus-to-pulvinar-to-temporal cortex pathway (Baldwin et al., 2017a,b). In primates, this second visual pathway is relayed from two nuclei of the inferior pulvinar to temporal cortex, now known as the MT complex (Kaas and Morel, 1993). The MT complex consists of the middle temporal visual area (MT) bordered by the MT crescent (MTc), the middle superior temporal area (MST), and dorsal and ventral fundal areas of the superior temporal sulcus (FSTd and FSTv). These areas provide the major visual inputs into the “dorsal stream” of cortical sensory processing that informs posterior parietal cortex and provokes motor behavior (Kaas et al., 2018). Except for MT, these areas all receive visual information from the superior colliculus via the two nuclei of the inferior pulvinar. Instead, MT gets its visual information directly from V1, and indirectly from V2 and V3. Thus, in primates, including humans, the dorsal stream gets information from both thalamic pathways to cortex. Because MT provides a source of V1 information to the dorsal stream that is not present in non-primates, motor behavior is much more dependent on V1 as a source of visual information. The cost is, of course, that lesions of V1 impact both on object recognition and on visuomotor behavior, but the gain is in the more detailed visual information provided by V1. It appears that inputs from V1 into the superior colliculus-pulvinar territory of temporal cortex in early primates or their immediate ancestors, defined a new visual area, MT, that is a dorsal stream area in temporal cortex that is unique to primates. Thus, MT evolved from cortex that was activated by a pulvinar relay from the superior colliculus in early mammals, but came to be activated by V1 in primates. Another important difference in primate brains from other mammals is in the distribution of cortical neurons. All primates have more densely packed neurons in neocortex than other mammals (Gabi et al., 2010). All primates also have a much higher packing of neurons in V1 than in other cortical areas, and this has been known for some primates for some time (Rockel et al., 1980). In order to pack in more neurons, neurons need to have an average smaller size, and this is clearly the case for neurons in V1 of primates, especially in layer 4. We now know much more about the distribution of neurons in neocortex and other parts of the brain for many species and taxa because of the studies of Herculano-Houzel (2016) and the studies that she provoked. In brief, neuron packing densities in primates are higher in V1 than in other cortical areas, they are also high in adjoining secondary visual areas, they may be somewhat higher than average in primary somatosensory and auditory areas, and they can be quite high in granular prefrontal cortex. Regional differences across the cortical sheet also occur in other mammals, but they are slight, and somatosensory cortex may have more densely packed neurons than visual cortex (Herculano-Houzel et al., 2013). The pattern of areal differences described here for primates is most weakly expressed in strepsirrhine primates, judging from galagos, and more so, but variably across New World and Old World monkeys and baboons (Young et al., 2013). The areal and regional variation in neuron packing is great in chimpanzees (Collins et al., 2016) and presumably in humans. Thus, it appears that the overall pattern of the variation in neuron packing densities was more even across cortex in early primates and not that much different from other mammals, but increased as

4 Early primates and other archontoglires

anthropoid primates emerged, and increased further with the evolution of apes and humans. This variation is important because it is part of the specializations of cortical areas for different functions. Partly because of the longer connection distances for axons in larger brains, the larger human brain has many larger neurons, reducing overall packing densities, but human brains also have extremely small neurons, the koniocellular neurons in sensory areas, resulting in extreme differences in neuron sizes. One of the advantages of big brains is that they can have bigger or more cortical areas, or both. Having more cortical areas allows areas to become more specialized for certain functions, rather than being constrained by the need to be multifunctional (Kaas, 1989). Sensory areas are often big in big brains, and there is an advantage in preserving the information in sensory inputs in great detail. This function is reflected in the sizes of neurons and their dendritic arbors. Large arbors sum many inputs, and produce outputs that reflect this summation. Small neurons with small dendritic arbors are predominantly responsive to only a few inputs, and thus the information in a few inputs is preserved, and can be processed in different way in different cortical processing stream (Kaas, 2000). V1 of primates tends to grow with cortical size, but this growth has a limit in the great apes, as humans do not have a notably larger V1 (Frahm et al., 1984), although considerable variation in V1 size has been reported for humans. In primates, V1 has very small neurons in layer 4, which preserve the information in inputs from the lateral geniculate nucleus, and smaller pyramidal neurons in layer 3, where their outputs to other areas of cortex use different inputs to start to form different processing streams. Four different outputs from V1 activate four different band-like repeating modules in V2, which provide major outputs to V3, DM, and MT (see Kaas, 2012). But, V1 has other functions that require large neurons with extensive dendritic arbors that sum many inputs from other V1 neurons. In particular, the very large Meynart pyramidal neurons that are small in number but have large receptive fields, sum information and project to MT and the superior colliculus (Fries et al., 1985). Thus, large cortical areas are more likely multifunctional, while small areas can be specialized, but less likely have functionally contrasting specializations. Motor cortex lacks an obvious layer 4 of small neurons, and is specialized for summing information by having large pyramidal neurons with large dendritic arbors. In contrast the small layer 4 neurons of granular prefrontal cortex are ideal for preserving information. We see the starts of these specializations in the neocortex of small strepsirrhine primates, and these beginnings of neuron specializations are greatly enhanced in monkeys, apes and humans. Another issue that is based on the increasing number of neurons in neocortex relative to the brainstem and spinal cord as one considers non-primates, small strepsirrhine primates, monkeys of various sizes, apes and humans is the probable consequences of subcortical targets having more and more of their inputs from cortex. When neocortex is damaged, the consequences of the loss of cortical inputs to subcortical structures are greater in humans (Herculano-Houzel et al., 2016). This may be, to a large part, because the subcortical neurons lose proportionally more of their activating connections, and are more impaired as a result. Thus, the

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longstanding evidence that cortical lesions impact on behavior more in humans and other big-brained primates than in other mammals, led to the concept of the corticalization of function in humans. Subcortical targets of cortical neurons may also change in other ways. One example is that in macaque monkeys (Rathelot and Strick, 2009) and presumably other anthropoid primates with skilled use of the hand, motor cortex has many neurons that project directly to the motor neurons of the spinal cord that innervate muscles that control the hand. These connections likely provide improved control of independent movements of the digits.

5 What about tarsiers? Tarsiers represent an odd line of evolution in the primate radiation. Their overall small size and strange body confused early investigators, and tarsiers were grouped with lorises, galagos, and lemurs as prosimian primates, that is, below the monkey (simian) level. That classification has now been changed, and the molecular evidence places them as an early surviving branch of the anthropoid radiation (Ross and Kay, 2004). What is unusual about the evolution of tarsiers is that early anthropoids were diurnal and specialized for daytime vision, and the tarsier line started off as diurnal, having lost its specializations for nocturnal vision, but then returned to nocturnal life by re-specializing for dim light. This largely consisted of evolving huge eyes relative to the head. Consistent with their reclassification, the dorsal lateral geniculate lamination pattern of tarsiers is clearly of the anthropoid type, rather than of the strepsirrhine type (Wong et al., 2010). Interestingly, the primary visual cortex, V1 of tarsiers is proportionately greater than almost any other primate at 20% or more of all visual cortex. As an extreme visual predator of insects and other small prey, tarsiers depend on a large V1 for the detailed representation that is needed for this function. As tarsiers are small, and have small brains, this dependence on a large V1 may have cost them in number of cortical areas. They have a V2 and MT and likely other visual areas, but little posterior parietal cortex and little prefrontal cortex.

6 Hominoids: Apes and humans Apes evolved from African monkeys over 30 million years ago (Murphy et al., 2004; Steiper and Seiffert, 2012; Steiper and Young, 2008). Early apes closely resembled African monkeys, except of course they had no tail. Apes were relatively successful during their first 15 million years or so, forming many species and spreading out over Africa and parts of Asia and Europe. With their slower reproductive rate, and the stress of short-term climate changes, apes were reduced to a few species of small numbers within rather restricted ranges. Present-day apes include gibbons, orangutans, gorillas, and chimpanzees. The “great” apes diverged from gibbons over 20 million years ago, and the African great apes from orangutans over 16 million years ago. Gorillas diverged from the line leading to chimpanzees and humans

6 Hominoids: Apes and humans

over 8 million years ago, while chimps and humans shared the common ancestors 6–8 million years ago (Fleagle and Seiffert, 2017). Humans have been extremely successful, now numbering many billions, and occupying much of the earth. This success is likely the consequence of our large complex brains, our ability to effectively acquire and use cultural learning relevant to different environments, modifications in our body for effective hand use and bipedal walking, and an increased reproductive rate, based on helpers to counter the long postnatal development of offspring (Boyd, 2018; Boyle and Wood, 2017). This success in some sense is both surprising and dependent on chance and unknown factors, given that all other species of hominids are now extinct. This includes a range of extinct earlier species with brains smaller than our own, but often considerably larger than the brains of present-day chimpanzees. Our close human relatives, the Neanderthals and Denisovans branched from the line leading to Homo sapiens some 700,000 years ago, and survived to recent times, overlapping the modern humans that emerged some 200,000 or more years ago. Neanderthals and Denisovans were capable of reproducing with modern humans, and these close relatives had brains as large or larger than ours. Why did these species or sub-species die out, while we survived in abundance? Moreover, why did most early lines of H. sapiens die out, such that present populations trace back to a common female ancestor, “Mitochondrial Eve” some 200,000 years ago (Bloch and Boyer, 2002). These ancestral humans arose in Africa and spread over the earth starting about 50,000 years ago, replacing those who left Africa earlier. Overall, much of this extinction may have been unrelated to differences in brain functions, and related to changing circumstances. However, our species (or subspecies) appears to form larger social groups, and this trait may have been favorable in displacing Neanderthals and Denisovans. As hominids evolved in Africa 6–7 million years ago, they had an ape-sized brain and an ape-like body, but had specializations for bipedal walking (Kozma et al., 2018) and altered use of the hand (Tocheri et al., 2008). We can assume that these early ancestors had brains with an organization much like those of modern chimpanzees. However, the organization of the brains of chimpanzees are not well understood due to limitations on the modern methods of study that have been applied to other primates. Even the non-invasive imaging methods that have been used to study human brains have been difficult to apply to chimpanzees. The chimpanzee has a neocortex about 35 times larger in surface area than the neocortex of macaque monkeys. Thus, the neocortical neuron numbers are much greater in chimpanzee than they are in macaque monkey. The primary and secondary sensory areas, as well as motor cortex, are much larger in chimpanzees, and these areas can be identified histologically (Bailey et al., 1950; Collins et al., 2016; Hackett et al., 2001; Qi et al., 2008). Thus, the sensory areas of the early stages of cortical sensory processing have been retained from monkey ancestors, and much of the organization of monkey cortex likely applies to ape cortex, since it also appears to apply to human cortex (Orban et al., 2004). In addition, other regions of cortex can be identified as similar to monkeys in histological structure (Bailey et al., 1950).

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However, the chimpanzee brain is clearly not just a larger version of a macaque monkey brain. Although the frontal lobe as a whole is not larger in chimpanzees than expected from the size of neocortex (Semendeferi et al., 1997), comparisons of “association” or higher-order regions of cortex to the sizes of sensory and motor areas indicate that some parts of cortex are disproportionally larger in apes and more so in humans, than in monkeys (Passingham and Smaers, 2014). Thus, parts of frontal, posterior parietal, and temporal cortex (association cortex) appear to be disproportionately enlarged. These same regions of cortex expand in the postnatal development of human brains, much more than sensory and motor regions (Hill et al., 2010). Another difference between apes and monkeys is that small differences in the shapes of the left compared to the right cerebral hemisphere in chimpanzees suggest a level of hemispheric specialization that amplifies brain function, although these differences are not as pronounced as in the more extreme specializations of the two hemispheres, most notably for language, that are seen in human brains (Gannon et al., 2005). All primates have higher neuron packing densities in neocortex than other large brained mammals have, but regional and areal differences in packing occur (e.g., Collins et al., 2010). However, these regional and areal differences are less pronounced in prosimian galagos, compared to monkeys. They appear to be more similar, but more pronounced in chimpanzees than in monkeys, with low neuron densities in motor and premotor cortex, and the highest levels in primary and secondary areas of neocortex (V1 and V2). High densities also occur in primary somatosensory cortex and dorsolateral granular frontal cortex (Collins et al., 2016). These differences in packing densities relate to average neuron size, and thus directly to the functions of cortical areas (Kaas, 2000). Other areas of insular and cingulate cortex in apes and humans have substantial numbers of the large Von Economo neurons that may involve special functions in these primates (Nimchinsky et al., 1999). Although Von Economo neurons were thought to be present only in apes and humans, they have more recently been described in agranular insular cortex of macaque monkeys (Evrard et al., 2012). Early members of the hominid (bipedal) radiation were varied but relatively small compared to humans, and had brains the size of chimpanzees (460 cm3). As brain sizes did not change substantially over a period of millions of years, we can assume that major changes in brain organization and functions also did not occur. However, fossils from East Africa with larger brains and more human-like teeth from east Africa have been dated to around 2 million years ago; and since that time the possible ancestors of our species gradually increased in brain size from roughly 600 cm3 in Homo habilis, 900 cm3 in Homo erectus, and 1200 cm3 in early H. sapiens to a range around 1400 cm3 in modern humans (De Sousa and Cunha, 2012). It seems likely that this transition from a very slow rate of increasing brain size to a more rapid rate depended on an extensive use of stone tools and other tools, more flexible foraging strategies that included meat eating, and the processing of food by cooking and pounding to make nutrients more accessible (HerculanoHouzel, 2016; Wrangham, 2009). To make these behavioral changes, brains of

6 Hominoids: Apes and humans

the sizes of 600–900 cm3 must have been much more capable than those of early hominids, but it is not clear what changes made these abilities possible. Nevertheless, these behavioral changes provided the nutrients that larger brains require, and further increases in brain size to become possible. Human brains are metabolically costly, and it takes a lot of cultural experience and learning to meet this cost. Humans differ from other primates in having offspring with brains that require up to 20 years or more to mature, and have a long time of dependence on parents and others. Apparently, it takes a long time for our species to produce a brain that is fully operational, and then it is only highly functional within a specific culture. This suggests that the most important changes in the brains, as they evolved to be modern human brains, were those that allowed them to acquire vast amounts of hard-earned learning (Murray et al., 2016). Language is a unique human accomplishment that is completely dependent on new features of the human brain. First, the neural mechanisms that mediate language are highly lateralized to the left cerebral hemisphere. The major advantage of such an arrangement is that it avoids the need for massive connections between the two hemispheres, which would be costly in conduction time, energy, and bulk (Hofman, 2014; Kaas, 2000; Ringo et al., 1994). Language appears to depend on sub-networks that were derived from cortical networks for object recognition and action that emerged in early primates, the so-called ventral and dorsal streams of processing for vision (Goodale and Milner, 1992) that have been joined by auditory and somatosensory components. The dorsal stream for language production (Hartwigsen et al., 2016; Sammler et al., 2015) resembles the other parietal-frontal networks for specific actions. Like networks for reaching, body and head defense, hand-to-mouth, and running (Kaas and Stepniewska, 2016; Kaas et al., 2018), these actions and speech can emerge so fast that we are little aware of the decision-making process, but not surprised by the outcomes. The ventral stream of language processing is more involved in word recognition, and the amount of memory and effort that is takes to acquire language is best appreciated as one learns a second language as an adult. Obviously, the brains of children have been primed in some way to have great interest in language as part of a larger need to learn from parents and others. Over thousands of years, there must have been selection for brain changes that improved the learning of spoken language, as those who learned earlier and more rapidly, likely had a reproductive advantage (the Baldwin effect) (see Pinker, 1997). Acquiring a written language (reading) is much more difficult, and it requires years of formal training. Speaking and reading appear to be examples of skills that highly depend on brain plasticity, as the appropriate cortical circuits are formed over years of experience. Recent functional imaging studies of word recognition in humans provide some suggestion of how hard-to-learn abilities depend on modifying brain regions so that they mediate new functions. As in monkeys, humans have a core of primary auditory areas bordered by a belt of secondary areas, and a parabelt of still higher levels of auditory processing (Hackett et al., 2001). In humans, a region of cortex in or just outside the auditory belt responds selectively to words, compared to non-words (Wilson et al., 2018). More caudally, a strip of cortex responds well to spoken words,

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but equally well to written words. More caudally yet, cortex is activated by written words, but not spoken words. As reading is an ability that emerged in only some cultures, and in recent times, we did not evolve reading areas of the cortex. Instead, with much training, an auditory region of the temporal lobe was modifiable to the extent that it could be used for spoken word recognition, along with learning induced modification of an adjacent visual region to recognize written words, instead of, or in addition to, other visual objects. A related example is in cortex called the face area in humans (Hoffman and Gauthier, 2007). Face recognition is exceptionally good in humans, and a region of cortex in humans is best activated by seeing faces. Thus, we can recognize hundreds and perhaps thousands of individual faces (Jenkins et al., 2018), something that is very important in our highly social species. Macaque monkeys also have face selective regions in temporal cortex (Freiwald and Tsao, 2010), showing that identifying individuals is very important in their social lives. But, while the face area in humans is naturally selective for faces it can be activated by other objects that require individual recognition and experience. Thus “experts” in identifying the makes and years of cars, or individual cows of the herd they tend, activate the “face” area of cortex when identifying cars or cows (Hoffman and Gauthier, 2007). Likewise, parietal-frontal networks for grasping and manipulation that we see in monkeys may have been enlarged and subdivided in the evolution of humans to allow skilled tool making and use (Kaas and Stepniewska, 2016; Kaas et al., 2018). Finally, it is important to recognize that the human brain is different from other primate brains in many ways. Neocortex in humans is very large and contains more neurons than the neocortex of any other mammal (Herculano-Houzel, 2016). This neocortex has many more cortical areas than the neocortex of macaque monkey (Van Essen et al., 2012a,b), and some of the areas of the two hemispheres are markedly different in function. Regions of cortex with cognitive functions are preferentially expanded (Hill et al., 2010). Recent books have covered the evolution of prefrontal cortex (Passingham and Wise, 2012) and memory systems (Murray et al., 2016). Yet, studies of the cognitive abilities of chimpanzees in comparison to even young children indicate that there are many gaps to fill. For example, human children have a much greater understanding of how everyday objects can be used as tools, and how to use them without training; while chimpanzees acquire such abilities with great difficulty and much training (Povinelli, 2000). As another example, humans work extensively together and share, while such social behavior is very limited in chimpanzees (Warneken et al., 2011).

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