Evolution of the Posterior Parietal Cortex

Inhalt

Abstract

Introduction

Materials and Method

Discussion

References

Appendix

Abstract

Current research on the Posterior parietal cortex in primates has difficulty accommodating the inferior parietal lobule (Husain & Nachev, 2007). In this study neuroanatomical data from human and non human primates is used to investigate the evolutionary changes in the primate posterior parietal cortex (PPC); specifically the Inferior parietal area. All species were tested using three different investigations. One investigation included comparing the whole volume of the PPC against the volume of the whole cortex, a second comparing the volumes of the internal subdivisions of the PPC, more precisely the superior parietal lobule (SPL) and the inferior parietal lobule (IPL) against the volume of the whole PPC. The third investigation involves comparing the volume of individual structures against the volume of their respective hemispheres (e.g. the left hemisphere of the SPL against the volume of the entire SPL). 27 in vivo primate brain scans were analyzed in total using MRI scans from six different species including humans, great apes and monkeys. Image analysis software was used to calculate total brain volumes. Allometric regression analysis was used to compare the relative volumes of brain structures across species, in order to determine whether human brain segments corresponded with predicted evolutionary trends based on nonhuman primate allometric trajectories. Analysis supports the prediction that humans and great apes show an increased volume within in the PPC in comparison to monkeys. Findings did not support this papers predication that the human IPL; specifically the left hemisphere, would be greater in volume compared to non-human primates. However, findings indicate that the left IPL has increased in volume among humans and great apes samples, in comparison to capuchin and macaque monkeys. The findings of this study

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provide additional insight into the evolution of the human brain beyond what is shown by volumetric analysis, by indicating the unique and exciting modifications in the human brain over the course of evolution. These modifications may represent some of the neurobiological changes which support human specializations in cognitive and behavioral abilities.

Introduction

Background

The PPC is involved in the instigation and guidance of different types of actions including reaching and grasping for objects, defensive movements and gaze direction (Kass, Gharbawie & Stephiewska, 2011). As well as these essential tasks, the functional streams for a variety of ethologically relevant behaviours start in the PPC (Kass et al, 2011). The PPC receives input from the three sensory systems that are involved in the localization of the body and external objects in space: the visual system, the auditory system and the somatosensory system (Panda & Seltzer, 1982). In turn, much of the output from the PPC goes to areas of frontal motor cortex: the dorsolateral prefrontal cortex, areas of the secondary motor cortex and the frontal eye field (Panda et al, 1982), all being fundamental processes in the development of higher order functions.

Damage to the PPC has shown to produce a variety of somatosensory deficits, including deficits in perception, memory of spatial locations, in accurate reaching and grasping movements, in the control of eye movements and in attention (Panda et al, 1982). There is

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also some evidence that the PPC is involved in the perception of pain (Witting, kupers & Svensson, 2001), language and even aspects of long-term memory (Shannon & Buckner, 2004) and many of its behaviours described constitute major notions of what it is to be human (Shannon & Buckner, 2004).

It is well recognized that the primate brain underwent dramatic expansion over the course of evolution (Jerison, 1973). However, not all brains have expanded equally (Preuss, 2001) and differences between humans and primates are not related to size differences alone, but also to the existence of internal cytoarchitecture, reorganization, loops or modules of individual brain areas (Barton & Harvey, 2000). Similarly, the PPC is an expanded area of cortex in humans, but also in other primates (Kass et al, 2011). Some argue that while the PPC has expanded in all primates, elaboration and differentiation of areas within the PPC is likely to occur in most primates, but this is especially true of humans (Kass et al, 2011). These neurological advances are believed to lead to uniquely human behaviours and functions such as the development of language (Kass et al, 2011). This paper investigates whether the PPC is disproportionately larger in humans - and primates similar to humans; the great apes. It also considerers the cherished association between uniquely human characteristics and a uniquely large human PPC, adding insight to this debated evolutionary association.

Many anthropologists, evolutionary psychologists and researchers alike are interested in understanding the source of the cognitive and behavioural differences between humans and non-human primates, and also between apes and other primates (Rilling, 2006). Researcher are interested in why is it that apes, in comparison to other non human primates, have a

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better understanding of aspects of social cognition such as self-awareness (Gallup & Swarez, 1981), components of theory of mind (Tomasello, Call & Hare, 2003) and capacity for symbolic thought (Savage-Rumbaugh, 1986). Investigations seek to uncover why is it also that humans are more advanced in areas such as language, reciprocal exchange, theory of mind, tool use, mathematics and artistic expression (Rilling, 2006). To answer these questions the brain should be investigated, observing for similarities and differences between humans, and other non-human primates. Comparative studies of humans and non-human primates are not only beneficial from an evolutionary perspective, but also because certain species (e.g. macaque or baboon) are genetically similar to humans, making them excellent animal models for scientific research (Falk, 2007). One way to investigate this similarity is to compare species that are thought to represent stages or grades that occur over the 65 million years of primate evolution (Falk, 2007). From this perspective one can compare anatomical structures or behaviors across appropriate representations from species e.g. prosimian -> monkey -> ape -> human (Falk, 2007).

Analysis of the primate brain

The examination of primate brain evolution has been, so far, examined in two different ways. One way to explore primate brain evolution is through the direct method. This method involves examination of fossilized brain casts that give an estimate of brain volume in cm3 (as well as brain mass in grams). The second method uses more modern indirect methods which comprise of electronically calculated analyzed through 3D computer topography (Falk, 2007). The indirect method of studying primate neuroanatomy has a

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variety of investigative techniques to answer questions regarding primate evolution. It answers to questions regarding type, size, density and distribution of cortical areas within regions of the cerebral cortex. (Preuss & Goldman-Rakic, 1991). This affords answers to neuroanatomical questions such as whether or not, (or how) additional cortical areas may have arisen during primate evolution, and to what degree they have contributed to an increase in primate brain size (Preuss & Goldman-Rakic, 1991). Whereas CT scanning is suitable for fossil material, magnetic resonance imaging (MRI) suits imaging of soft-tissue structure non-invasively and in vivo. PET and fMRI are also commonly used measures for studying neuroanatomical structure in primates (Semendeferi et al, 2001). Although these measures are more sophisticated, the logistics of synthesizing findings from primate brain imaging can be difficult.

When quantifying primate brain sizes, certain allometric factors guide the general internal and external morphology. Larger primate brains are distinguished by more sulci and gyri convolutions than smaller ones (Radinsky, 1975), which seem to be a mechanism for sustaining the ratio of surface (cortex) area to brain volume as brain size increases (Jerison, 1982). Neuronal density decreases with increased brain size, however, mean neuronal size does not appear to scale allometrically with brain volume (Haug, 1987). Compared to other mammals, the primate cerebral cortex is thicker with more highly granulated areas (Haug, 1987). The volume of grey matter is basically a liner function of brain volume, whereas the mass of interconnections which form the underlying white matter increase disproportionately with brain size (Hofman, 2001). These findings add to controversies regarding the internal architecture of the primate brain (Hofman, 2001). This paper investigates controversies in this area and seeks to enlighten this old neuroanatomical debate.

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Primates are known to possess 50-100 highly convoluted cortical areas, and it has been hypothesized that many of these may be higher-order areas which are unique such as dorsolateral prefrontal, inferior-temporal and posterior parietal cortices (Preuss, 1999). These unique system represents a natural by-product of increasing brain size, and coincides with research by Ringo (1991) who suggest that enlarged brains would mechanically become swamped with white matter without neurological reorganization that increase the number of local (as opposed to longer corticocortical) connections, and therefore areas. The addition of these new cortical areas and connections may have provided the opportunity for the evolution of new behavioural capacities (Preuss & Goldmann-Rakic, 1991).

Comparative work investigating the cerebellum, known to be important in motor co-ordination and now thought to contribute to higher cognitive abilities in humans (Muller et al, 1998) underwent neurological reorganization during primate evolution. Thus, the lateral cerebellar system is comparatively large in chimpanzees and gibbons, while a central nucleus is larger in humans than apes (Matano & Harasaki, 1997). This is particularly interesting given the fact that the human cerebellum appears to be smaller than would be expected in an ape brain of human size (Semendeferi & Damasio, 2000). Significant research, separating humans from chimpanzees to an extent which rivals the degree of separation between new world and old monkeys and apes, implies that the internal organization of the human brain is qualitatively different from that of other living primates (Oxnard, 2004). Contrary to previous theories of independent functional neurological systems (Barton & Harvey, 2000) the fore mentioned research entailing distributed structures across multiple modules within the brain is supported by fMRI studies. These indicate that higher-order cognitive tasks engage a number of cortical areas which connect across the cortical mantle (Frackowiack et al, 1997;

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Semendeferi & Damasio, 2000; Semendeferi, 2001). However, research in this area remains underdeveloped, and the underling neurological question of where (and how) evolutionary expansion within the cortex leads to species-specific behaviours remains unresolved (Semendeferi & Damasio, 2000).

One way to examine these neurological expansions has been to observe for increases in absolute brain size between species (Gibson, 2001). Absolute brain size is extremely variable across living primates. For example, in living prosimian, monkeys and gibbons overlap and together range between 1-205 cm3 , which is distinct from the great ape range between 275-752 cm3 (Falk, 1986) (see tables 1a,b). The human range is above this further, typically ranging from about 1100-1700cm3. In addition to this fact, researchers questioned how certain primates, e.g. the pygmy mouse lemur, which has a body weight of approximately 30g, be compared to much larger primates such as apes. A more meaningful parameter was needed between body weight and brain size. Jerison (1973) was the first to partition the respective total increase in brain size for different groups of primates into two parts: those associated with allometric scaling expected for their body size, and any remaining increases (or decreases), known as residuals. In 1972 Jerison introduced his now famous encepalization quotient (EQ) to resolve this troubling issue. EQ is a measure of relative brain size defined as a ratio between actual and expected brain mass (Jerison, 1972). EQ uses brain/body weight data from living mammals to establish a baseline regression with the formula:

EQ = Ei/0.12Pi .67 ; where Ei = actual brain size, and Pi = predicted brain size, and 0.67 is the exponent. The exponent of 0.67 follows a power law governing the body-size to surface-area relationship (Armstrong, 1983). However, other researchers have more recently taken on the exponent of 0.75; among which the most notable was Martin (1982), as this also accounts for

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several physiological variables in brain size. Humans are known to have a high EQ value, as are capuchin monkeys (Stephan et al, 1970). Gorillas on the other hand have a lower EQ value than would be expected for a primate of their body size (Stephan et al) (see table 2).Due to this and other research, it is now known that EQ in extant species have brains and (separately) neocortices that are roughly three times larger than expected for nonhuman primates of the same body size (Stephan et al, 1970; Passingham,1973). Surprisingly, this is also true when using regression equations based on all nonhuman primates, just monkeys and apes, or apes alone (Stephan et al, 1972). This paper investigates EQ in primate brains based on research by Jerison (1972), expanding knowledge in this area.

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Table 1(a):

Absolute brain volumes based on research by Falk (1986).

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Table 1 (b)

Ranges of cranial capacities in living primates, excluding far-reaching extremes in humans for comparative purposes (modified from Falk 1986).

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Table 2:Table of EQ vales based for primates based on research by Jerison (1973) and Martin (1980)

Controversy remains however, on whether brain size alone can account for the observed diversity in primate behavior given the increasing evidence for suggested individual circuitry, neurochemistry and subsystems (modules) reorganized within brains to accommodate evolving behavior repertoires (Preuss, 2004; Holloway et al, 2004; Preuss et al, 1999). Holloway (1979) was particularly influential in emphasized the important evolution of cortical reorganization, emphasizing the qualitative relationship between brain nuclei, fibre tracts and neuroreceptor cites, thus giving consideration toward rewiring and altered

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neurochemistry in brains of similar (or different) sizes. This consideration is especially important when considering EQ values in primate brains and species-specific differences in behaviour (Holloway, 2004; Preuss, 2001). Gibson (2001) investigates species-specific differences in mental flexibility using a test known as The Transfer Index test. Gibson (2001) argues that absolute brain size, body weight and extra neuronal density all correlate with performance on the test, while EQ does not. Gibson (2001) states that the most practical measure for distinguishing intelligence and predicting human-like higher cognitive functions in hominids is absolute brain size. These insights are undoubtedly important neurological aspect in the broader understanding of primate brain evolution. This paper attempts to assist toward a resolution of this evolutionary brainteaser (pun intended, sorry!) and a sensible place to being is an area that is known to be involved in many uniquely human characteristics such as language and advanced tool use (Peeters et al, 2009) the PPC.

Research suggests that primates possess a unique PPC compared to other species (Kass et al, 2011). The primates branch of mammalian evolution known as Euarchontoglires (Kass et al, 2011) expanded over the past eighty to ninety million years producing present day primates as well as close relatives to primates including rodents and lagomorphs (Murphy et al, 2001). Studies on rodents, lagomorphs, and tree shrew indicate that primates derived from ancestors that had little PPC (Disbrow et al, 2007). Thus, the PPC was not as important a part of the cortex that it is in most primates today (Kass et al, 2011).

Since the PPC was only a small portion of the cortex, it was thought to have a more limited role. Rodents such as rats and squirrels also have quite small PPC’s and have direct visual and somatosensory inputs into the motor and premotor cortex (Kass et al, 2011). Therefore,

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an expanded PPC with individual modules and connections with the motor and premotor cortex form parallel networks which support different actions (Kass et al, 2011). These patterns emerged as early primates evolved, and their fundamental parts have remained in most, or all, extant primates (Kass et al, 2011). This paper will analyze this evolutionary enlargement in the primate brain using modern neuroanatomical techniques.

The PPC; Location and functions

In primates the PPC is located between the sensory motor fields around the central sulcus and the visual areas found in the posterior occipital cortex (Grefkes & Fink, 2005). The PPC can be subdivided into the Superior parietal lobe (SPL) (Brodmann areas 5 and 7) and the inferior parietal lobule (Brodmann areas 39 and 40) separated by the interparietal sulcus (Mishkin & Ungerleider, 1982). However, Brodmann did not identify areas 39 and 40 in monkeys (McFay, 2007). Whether monkeys have areas homologous to human area 39 and 40 remains controversial (Radinsky, 1975). Brodmann (1909) suggested that the homologues of the cytoarchitectural subdivisions of the monkey PPC (areas 5 and 7) are both situated in the human superior parietal lobule, and that the human IPL (areas 39 and 40) is an evolutionary new area (Peeters, Simone, Nelissen, Fabbri-Destro, Vanduffel et al, 2009). Research by (Peeters et al, 1982) indicates that while the IPL is functionally similar in humans and non-human primates, the rostal part of the IPL is a new area in humans which is not present in monkeys. They propose that this area is needed for manipulating hand actions, specifically in advanced tool use (Peeters et al, 1982). This view has not been

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confirmed by other researcher, and recent literature has begun naming the IPL architecture in non-human primates as similar to humans (Pandy & Seltzer, 1982). This paper seeks to clarify discrepancies in the literature regarding the evolution of the PPC and its subdivisions; specifically the IPL, and to investigate whether the IPL has developed more in humans.

Most of the evidence gathered indicates that subdivisions of the PPC are involved in co-ordinating different actions (Kass et al, 2011). A central region of the cortex of the intraparietal sulcus in macaques, the parietal reach region (PRR) appears to be associated with reaching (Batista et al, 1999). The lateral intraparietal region (LIP) appears to be associated with gaze direction (Colby et al, 1998), and the anterior intraparietal region (AIP) appears to be involved with grasping and manipulating objects (Sakata et al, 1995). More recently, the ventral intraparietal region (VIP) has been associated with defensive movements of the head and arm to protect the head (Cooke et al, 2003). (See figure 1). Data collected by Grefkes & Fink (2005) indicate that anterior areas of the IPS, containing areas AIP and VIP are relative homologous across species. In contrast, posterior areas such as LIP and CIP, have been located more medially in humans, possibly reflecting differences in the evolution of the dorsal visual stream and the IPL (Grefkes et al, 2005) (see fig. 2). Connections from the visual areas are mainly restricted to the inferior half of the PPC (Fang et al, 2005) and, in contrast, the superior half of the PPC receives many inputs from the somatosensory cortex (fang et al, 2005).

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Fig. 1: Lateral view of a macaque brain with the Intraparietal sulcus (IPS) opened up. MIP = medial intraparietal area, CIP = caudal Intraparietal area; LIP = Lateral Intraparietal area; AIP = Anterior Intraparietal area; VIP = Ventral Intraparietal area; POS = parieto-occipital sulcus; LS = Lunate sulcus; SF = Sylvian fissure (lateral sulcus); STS = superior temporal sulcus.

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Fig.2 Post mortem examination of a macaque and human brain. (taken from Zilles collection, C & O. Vogt institute of brain research, Dusseldorf University, Germany.

A .The sulcus anatomy of a macaque brain is much less complicated than the highly gyrified cortex of a human brain. The IPS in humans often has various side branches (indicated by the asterisks in A) and indicates a complex folding pattern

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Logic behind current research

This paper seeks to resolve discrepancies in this area by investigating the development of the PPC in primates. Volume differences in the primate PPC and its functionally specific zones; the IPL and SPL will be investigated. A focus will be maintained on the IPL. Findings will be used to indicate species-specific evolutionary changes. Further to this, hemispheric differences in the IPL in humans have been noted to relate to deficits in action control leading to apraxia with left IPL lesions, and deficits such as hemispatial neglect after right sided damage to this area (Serrien, Ivry & Swinnen, 2006). Studies were conducted in both humans and monkeys. However, it was noted that human right sided neglect was far more prominent and long lasting than in macaque monkeys (Serrien et al, 2006). Studies of the parietal region indicate that individuals with left hemisphere lesions are likely to show impairments in skilled actions and movement complexity (Haaland, Elsinger, Mayer, Durgerin & Rao, 2004). Further to this, recent fMRI studies observing the left IPL in humans and macaques indicates that regions of the left IPL appear to be specific to humans for the use of tools (Peeters et al, 2009). Findings, indicated by activation of posterior parts of the human IPL when using tools such as rakes and pliers, were not replicated with macaques, even after extensive training in tool use and proficiency with rakes and pliers was established in monkeys (Peeters et al, 2009). This indicates evidence for the existence of a region of the left IPL unique to humans for the use of tools. Whether this region is due to the evolution of a new area, or simply duplication or enlargement of old one remains to be discovered (Zilles & Palomero-Gallagher, 2001; Sereno & Tootell, 2005). This paper attempts to gain a greater understanding of the difference in the IPL between humans and primates,

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and its individual hemispheres. It is proposed that the IPL will comprise a greater volume than its counterpart; the SLP in humans, due to human evolutionary pressures related to function. Also, it is predicted that a greater volume in the left hemispheres of the IPL will be observed in humans in comparison to non-human primates, relating to evolutionary differences in species-specific behaviour. It is proposed also that the volume of the PPC will be greater in humans and great apes, but especially humans, in comparison to other primates related to evolutionary advances of this area. Findings may in turn indicate a region for higher cognitive abilities in humans such as those described, including attention and aspects of long-term memory, or in great apes related to species-specific advances described, which are not seen in other non-human primates such as increased social cognition. Through this research an advance in current knowledge regarding the evolution of the PPC and its subdivisions in primates will be achieved, enlightening new research on the PPC and its role in species-specific functions and behaviours.

Findings and implications

In this respect, a comprehensive analysis of the volumes of the PPC and IPL, and their individual hemispheres in human and non-human primates is undertaken using three-dimensional (3D) reconstructions of magnetic resonance imaging (MRI) brain scans. In addition EQ, based on Jerison’s (1972) research, was examined to establish changes in allometric trends and used to make inferences from these comparisons. Findings support a pattern of evolutionary development in the volume of the PPC of human and great apes. No significant differences were noted between absolute volumes of the IPL in humans in comparison to other primates however. Differences in the volume of the left IPL in humans

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and great apes, in comparison to monkeys was found however. Greater volume in the right hemisphere of the SPL in humans was also indicated. These findings may indicate possible evolutionary expansion in this area related to advances in species-specific behaviours. EQ values established are also noted to be closer to those predicted by Martin (1980) and not Jerison (1973). (See table 2). The largest non-primate EQ value is found in capuchin monkeys and the smallest in the gorilla, coinciding with research by Martin (1980). This has implications toward current understandings in this field.

Materials and Method

Ethics Statement

This project was approved by the Royal Holloway University Ethics Department. Therefore quality and integrity of the research was sought and approved. All participants were voluntary and involved gave their signed consent to partake in the research project. No harm was caused to any participant or animal during this independent and impartial study.

Participants

We used scans of 10 living humans, 11 great apes including 6 chimpanzees, 4 bonobos and 1 gorilla. 4 new world monkey brain scans were used from capuchin monkeys and 2 old world Macaques. The human cases included 10 TI structural MRI scans from human participants from a previous study (please see Ethical Approval reference no 2007-055 in which the cases were used for a very similar comparative study of the cerebellum). Scans were acquired in the MRI Unit at RHUL. Participants had given informed consent before inclusion. Critical criterion for inclusion of human participants included being right handed and having normal or corrected-to-normal vision. Data was anonymised so that each participant’s identity cannot be determined from the scans (see table 3 for descriptives).

For non-human primate cases all T1 structural MRI scans were obtained from a previous study at the Yerkes imaging centre (Yerkes National Primate Centre, Emory University, USA). All data were acquired in accordance with the American Psychological Association

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guidelines relating to the ethical treatment of animals. This data is now publically available to download to researchers from the FMRI data centre. (www.fmridc.org/f/fmridc/77.html). The macaque and capuchin monkeys were used as an out-group comparison for character states within primates (see table 3 for descriptives).

Volumetric estimates

For each brain we obtained T1-weighted contiguous MRI coronal sections throughout the whole brain (1.2-1.6mm thick). All were reconstructed in 3D using FSLview, an interactive programme designed to reconstruct, segment and measure MRI images. The sulcal and gyral morphology were displayed in three planes of section simultaneously (mid-sagittal, coronal and horizontal view) on a computer screen. Anatomical masks were manually constructed for the whole area, left hemisphere or right hemisphere of the cortex, the PPC, the IPL or the SPL. Each area was masked individually. This involved manually creating masks through removing irrelevant areas from a coloured digital display which had been placed over the original MRI scans. For example, when masking the cortex, the cerebellum, pons, medulla and the greater area of the midbrain were removed from the coloured digital display. (Further segmentation procedure for each area is described fully below). Masks were started on the mid-sagittal image on which anatomical landmarks were more readily distinguished in different species. Any changes made to the mid-sagittal image were automatically tracked through to coronal and horizontal view slice of the image. Coronal and horizontal views were also used as a visual guide to refine the assignment of individual voxels to specific cortical areas. (See fig. 3). Once all areas were masked, FSL utilities were used to compute the total volume and voxel count for each region of interest.

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Figure 3.

Image of masked area of cortex in a human MRI scan indicating Mid-sagittal, coronal and horizontal view of masked human cortex from FSLview.

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Figure 4: enlarged image of masked area of human cortex with arrows indicating relevant removed areas.

The area of the PPC occupied by the IPL was computed by subtracting the volume of the SPL from the whole PPC using FSL maths. The volume of the left side of each hemisphere was

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calculated by subtracting the right side from the whole using also FSL maths. (For example, to compute the left hemisphere of the cortex, the volume of the right hemisphere was subtracted from the volume of the whole cortex, using FSL maths). .Following this volumetric estimates of the whole cortex, the PPC the IPL and the SPL were computed for all species using FSLstats. The volumes calculated within each traced region were produced in both voxels and cubic millimetres. For this study only voxel counts of marked areas were required. Our resulting volumetric estimates from brain samples using MRI have the advantage of being free of the effects of shrinkage following histological tissue processing. Previous studies have not allowed for this shrinkage effect and this may affect their results (ref). In vivo scans also have the advantage of being free from shrinkage related to autolysis time and preservation method.

Segmentation procedure Posterior parietal cortex. Major landmarks, common to all species, were used to separate the PPC from the rest of the cortex. On the 3D volume reconstruction the sub-temporal gyrus was identified on the lateral and medial surface of each hemisphere. The most caudal section of the PPC, the parieto-occipital sulcus was identified using the original coronal sections and was marked (See fig 4). From the sub-temporal gyrus on the mesial surface of the cortex the outer border of the post central gyrus was identified as the most ventral part of the PPC and marked. These landmarks formed the dorsal, orbital and mesial borders portioning the PPC from the rest of the cortex in all species. However, sulci alone are not enough to define homologous areas between species, as has been pointed out by previous research (Bailey et al, 1950 from the evol of the frontal lobes), and individual differences in the sulcus architecture in both human and non-human primates adds to the complexity (expand and talk about cytoarchitecture; should be in intro as well). Unlike the prominent landmarks used to

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identify the boundaries of the PPC, the choices of landmarks to accurately trace the PPC in all species required a combination of information about the homologies of sulcus patterns across species and the underlying cytoarchitecture of the cortex. The landmark of the inferior parietal zone of the PPC was marked by following the landmark of the post central gyrus toward the superior temporal gyrus. The superior temporal gyrus was traced through the supramarginal gyrus (Brodmann area 40) and angular gyrus (Brodmann area 39) and toward the parieto-occipital sulcus. In this manner we respect the cytoarchitectonic borders in all species. All other landmarks used were the same across species (see dig. 4).

The landmarks drawn in different colours on the 3D image of the brains were automatically transferred to the 2D serial sections, enabling tracing of the segments of the PPC seen in each section as a separate region of interest. All sections in which the PPC occurred were traced in this fashion.

Figure 5 Medial view of the masked area of PPC with arrows indicating relevant masking landmarks used.

Subdivisions of the PPC; the superior and inferior parietal lobes

The PPC was subdivided into two sections; the superior and inferior portions of the parietal lobes occupying the PPC. The choices of landmarks dividing these two sections were directed by the principle that they were present in all species. Based on previous research (Duvernoy, 1991), the intraparietal sulcus was marked as the dividing sulcus between inferior and superior parietal zones of the PPC. On the lateral surface, a line was traced from the posterior of the intraparietal sulcus through to the post central sulcus, and followed the landmark of the post central gyrus, marking the superior parietal region of the PPC. The inferior parietal region of the PPC was then removed, leaving only the SPL. Finally the two hemispheres for each traced area; the whole cortex, the whole PPC, the whole IPL and the whole SPL were marked individually.

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Figure 6 Masked image of the human superior parietal lobule with arrow indicating relevant landmark.

Statistical analysis

As noted previously, masked areas were analysed and total volume covered by each region of interest (ROI) was computed (see table 4). Each ROI was calculated as a percentage occupied within whole areas (e.g. the percentage of PPC occupied within the cortex of humans), giving relative as well as absolute values for each species ROI (See table 5).

Species were then categorised into 3 different groups according to their resulting cortical and PPC absolute values; group 1 = humans, group 2 = great apes (chimpanzees, bonobos and gorilla) and group 3 = smaller bodied monkeys (macaque and capuchins) (described further below). A total of 4 MANOVA calculations were then applied to establish an effect of area and laterality type on volume. Independent variables (IV) were region; Cortex, PPC, SPL and

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IPL, with three levels; Whole, left hemisphere and right hemispheres. Dependent variables (DV) were volumes. Significant effects of region and laterality on volume were found between species groups (see table 5(a) and 5(b)). Following this, absolute volumes of ROI were then converted to log values using spss, a mathematical computer programme for statistical analysis. Computing log values normalises data for easier analysis and tends to equalise the variance in the dependent variable across different values of the independent variable (Rilling & Insel, 1999). Linear regression analyses were then computed in log form to predict relationships between variables. Significant relationships were found between species groups (described in results).

Allometric relationships between variables were investigated be fitting a least squares regression line through bivariant logaritmitic plots, also known as log-log plots. Log-log plots indicate whether date is isometrically or allometrically scaled. A line of best fit through two separate sets of data allow measurement of the expected and actual values, determine if the scaled relationship in the data deviates from an expected relationship (Emerson, 1978). Because humans are obvious outliers with regard to relative brain size (Jerison, 1972), including them in the plot would considerably alter the slope of the line and the magnitude of the species residuals. Therefore a least squares regression line is fit through the non-human primate data first. The human reserved data is then added to the plot and a best fit line established, giving actual values (see figure 4). A least squares regression with 95% confidence interval is used. The fundamental allometric equation used is Y = mX + c, where Y = the volume of one part of the organism, X = the volume of the whole organism, or the volume of another part, m is the slope of the line and c describes how Y changes in respect to changes in X at the intercept of the Y axis. If m >1 (referred to as positive allometric relationship when X and Y are dimensionally equivalent), increases in Y outpace increases in

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X. If m < 1 (referred to as negative allometric relationship), increases in Y do not keep pace with changes in X. If m = 1 (an isometric relationship), the relationship is linear, and Y and X increase at the same pace. When log-transformed, the equation becomes log Y = log a + b log X, so that, when plotted on log co-ordinates, the function becomes a straight line with a slope equivalent to the value of the scaling exponent (b) in the power function.

However, predictions should never be made regarding the size of a structure based on the size of the whole brain (Deacon, 1988). Therefore the volume of whole structures (e.g. the PPC whole) was regressed against the volume of the area, minus the volume to be regressed (e.g. cortex whole minus PPC whole). Since a structure with a higher exponent comes to occupy a greater part of the whole brain as the brain expands in volume, the difference between the one species relative PPC value and another’s’ may be explained by differences in absolute size alone. Doing this would not completely imply differential expansion between species beyond expected allometry.

When the logged PPC is regressed against the logged cortex minus the logged PPC, the same regression line fits smaller brained primates and great apes, if humans are omitted from the regression line. The slope of this single line is less than 1, indicating that the PPC has been expanding in non-human primates sampled at a slower rate than the rest of the cortex (Russon & Begun, 2004). When humans are added to the plot they are visibly noted to be slightly above expected values (See figure 4).

EQ values for human PPC are calculate by substituting log values calculated for cortex minus PPC; whole area and left and right hemispheres, into X from our equation graph giving the expected value, which when divided by the X give EQ value for human PPC whole. Residual values were calculated using a 95% confidence interval and the amount, with humans falling

Evolution of the PPC 27

within the 95% confidence range in all cases. The amount of variance accounted for in the data is also computed (see table 6). Calculation was repeated for all ROI between species (see table 6).

Results

Absolute volumes

Overall, absolute volumes of ROI were greatest in humans and smallest in capuchins for all regions and hemispheres (see table 4).

Relative volumes:

In this sample bonobos have the largest relative volume of PPC, chimpanzees second, capuchins third and humans are fourth. The smallest relative PPC is seen in the gorilla. These results remain very similar for absolute volumes of both left and right hemispheres in each ROI (See table 5).

The bonobos is again found to have the largest relative volume of IPL, second largest is seen in our human sample, and the gorilla possesses the third largest relative IPL followed by chimpanzees. The smallest relative IPL volume is seen in the macaques and capuchins respectively. Results again remain stable with species when left and right hemispheres are calculated (see table 5).

MANOVA

Overall the MANOVA’s indicate that there is a significant difference in volumes between cortex; whole, left and right hemispheres and PPC; whole, and left and right hemispheres between all three categories, with humans indicating the largest mean cortex and PPC in all

Evolution of the PPC 28

cases. A significant difference was found between IPL: whole, and left and right hemispheres between humans and great apes, with great apes indicating the greatest mean volume for IPL whole. Humans had the largest mean volume of IPL in both the left and right hemispheres however. Monkeys indicated the smallest mean IPL volume in all cases. A significant difference was found between species categories for SPL. Humans are found to have the greatest mean SPL whole volume, and mean SPL left volume, followed by great apes and then monkeys. Monkeys are shown to have the greatest mean SPL right volume however, followed by humans and then great apes (see 5(a) and 5(b) for full MANOVA descriptive).

A multiple regression analysis was performed to predict log volume cortex whole from log value PPC. Species category was entered as the first variable in the block. The total regression model explained 87% of the variance on the log volume cortex whole. PPC volume significantly predicts cortex volume F(2,24) = 83.052, p < .001. B =.420.

Allometry

Data for ROI were analysed in terms of allometry by regressing whole structures (e.g. the PPC whole) against the volume of an area, minus the volume to be regressed (e.g. cortex whole minus PPC whole) on a log-log plot and a best fit line estimated with non-human primates. Reserve data was then added to the plot and a best fit line was applied (see fig. 5). Statistical test for slope and EQ values as described previously were conducted.

The PPC in humans was larger than expected for a primate brain of human cortex size (see fig 5). The slope is less than 1 indicating an allometrically weaker relationship. Therefore, increases in PPC volume are not in pace with increases in cortex volume in our sample. The expected PPC volume is outside the 95% confidence interval and therefore is a significantly

Evolution of the PPC 29

different from the observed PPC volume. On visual examination, human data are continually seen above the best fit line, giving further indication of the larger than expected PPC size within human data. Table 6 lists the (log) expected brain volume and the 95% confidence interval around the (log) value observed for each species. The human PPC is significantly larger than expected for a primate of our brain size.

Encepalization (quotient) (EQ’s) and residual values are given in table 6. EQ values for PPC are greatest in humans, and capuchins, followed by the chimpanzees and bonobos. Macaques have the second lowest EQ value for PPC and the lowest value is observed from the gorilla. The slope is less than 1 in all cases indicating an allometrically weaker relationship. The expected value for PPC is outside the 95% confidence interval for capuchins, macaques and gorillas. The capuchin PPC is significantly larger than expected for a primate of its brain size. The macaques and gorillas have significantly smaller PPC volumes than would be expected for primate of their brain sizes. Bonobos and chimpanzees fall within the 95% confidence interval indicating a PPC volume as significantly large as expected for a primate of their brain size.

The human IPL indicates a slope of less than one and is therefore an allometrically weaker relationship. Therefore increases in IPL volume are not in pace with increases in PPC volume. The expected human IPL volume is outside the 95% confidence range indicating a significantly larger than expected IPL of human PPC size. The left hemisphere of the human IPL also indicates a significantly larger left IPL than would be expected for a primate of their PPC size. The left IPL in humans also has the second highest EQ value seen in the human data (see table 6).

Evolution of the PPC 30

The slope in all cases for primate IPL volume is less than 1 indicating an allometrically weaker relationship. Therefore changes in IPL volume are not in pace with change in PPC volume in all species examined. The expected value for IPL is outside the 95% confidence interval for capuchins, macaques and gorillas. Bonobos and chimpanzees fall within the 95% confidence interval, indicating an IPL volume as significantly large as expected for a primate of their brain size (see table 6).

Overall, humans indicate a significantly larger than expected volume within all ROI for a primate of our brain size. Interestingly the largest EQ value in human data is seen in the right SPL, the second largest in left IPL. The lowest EQ value in humans is observed from the left and right PPC hemispheres. In primates, capuchin monkeys have significantly larger than expected IPL, SPL and PPC volumes for a primate of their brain size. Macaques and the gorilla have significantly smaller volumes of ROI for primates of their brain size while bonobos and chimpanzees keep pace in growth for all ROI within what is expected for a primate of their brain size.

The small sample size used in this study means these results should be taken tentatively as they only represent a small sample and cannot be generalised to all data. Nonetheless, these findings are significant and the observed data is remarkable.

Figure 4: Log-log plot of non-human data, with human residuals added. Log PPC is seen on the Y axis, Log cortex minus PPC is seen on the X axis.

Discussion

Findings: PPC

Overall humans have a greater absolute PPC volume compared to other species investigated. Great apes have the second largest volume and smaller bodied monkeys have the lowest absolute PPC volume. This is true of all of species sampled and accounts for both hemispheres. However, contrary to expectations it was not the most cognitively advanced species where we found the largest relative PPC; a structure known to be heavily involved in tasks such as movement, attention and memory (Kass et al, 2011). The largest relative PPC was observed among the great apes; the bonobos. The second largest relative PPC volumes was seen in the chimpanzee, supporting one of this papers hypothesis that great apes and humans would have a larger PPC than smaller bodied monkeys sampled. However, it was not

Evolution of the PPC 32

proposed that great apes would have a greater relative volume in comparison to humans. Previous research by Tomasello et al (2003) has investigated the PPC in great apes. Their findings indicate that great apes have an increasingly evolving PPC (Tomasello et al, 2003) and they relate their findings to evolutionary advances in cognitive functions, social cognitions including theory of mind understanding and social awareness skills. Similar findings are not replicated in monkeys (Tomasello et al, 2003). Findings from this study should be taken tentatively due to the small sample size involved. However, results are notable and findings indicate that humans do not have a larger PPC in comparison to great apes. The smallest relative PPC is seen in the gorilla. However, due to only having one sample, this finding is preliminary at best. The small mean for this species relative PPC may indicate a possible outlier in our data. Another surprising finding is the relative volume of the PPC in the capuchin monkeys. The capuchins possess the third largest relative PPC volume of the species investigated. Our findings should be viewed as preliminary until a larger sample of gorillas and capuchins can be investigated. Nonetheless, results remain relatively stable across species when examining relative PPC laterality also (see table 5), indicating some homogeneity within samples.

Further analysis based on allometric relationships indicates the human PPC volume to be outside the expected range for a primate of our cortex size, and an allometrically weaker relationship between human PPC growth is indicated. Increased in growth rates for the human PPC were not in pace with the cortex, indicting the human PPC to be significantly larger than expected for a primate of our cortex size. These findings support research by Husain & Nachev (2007) regarding the evolution of the PPC in humans which indicates the continuing expansion of this area related to species-specific functions and behaviours.

Evolution of the PPC 33

IPL

Findings from total volumes in the IPL again indicate that humans have a greater absolute IPL volume than any of the other species investigated. Great apes have the second largest absolute volume and smaller bodied monkeys have the smallest absolute volume investigated in this research (see table 4). These findings are supported by previous research investigating the IPL in humans (Peeters et al, 2009). Relative IPL size in the humans was comparatively large; the second largest of all species sampled. This is contrary to this papers hypothesis and goes against previous research by Peeters et al (2009) who indicate findings for a larger IPL in humans.

Peeters et al (2009) relates findings to an evolutionary expansion in the posterior area of the IPL; the aSMG. This is thought to have occurred due to advanced skills including the advanced use of tools and is cited as being unique to humans (Peeters et al, 2009). The greatest relative IPL volume was observed in the bonobos, this has not been found in previous research. However, this is one of the first papers to investigate the evolution of the IPL in great apes. These results may indicate the evolution of the left IPL as a hominoid trait, rather than human alone. These results should be taken tentatively due to a sample of only four bonobos. Results are remarkable however and finds for future consideration cannot be ruled out. In line with previous research, chimpanzees and the gorilla have the second largest relative IPL volume, with capuchins and macaques possessing the smallest (see table 5).

When the left side of the IPL is investigated, findings indicate that humans have the greatest overall volume in comparison to all other primates. This is not a new discovery however and has been noted previously (Falk, 1986) (see table 1(b)). When the relative size of the left IPL was examined, findings did not support this papers hypothesis and humans were not found to

Evolution of the PPC 34

have a larger left IPL compared to non-human primate data. This is goes against current theories on the growth of the left IPL in humans related to functions of advanced manipulation of objects, handedness and advanced tool use (Peeters et al, 2009). A number of studies also indicate the role of the left IPL in behaviours including gaze direction (Colby et al, 1998), reaching and grasping for objects (Sakata et al, 1995) and defensive movements of the hands to protect the face (Cooke et al, 2003). Most of these studies were conducted between humans and macaque monkeys however, therefore the possibility that great apes possess an expanding left IPL remains undiscovered. This paper assists towards a better understanding of this issue. A substantial sample of human MRI scans were analysed, supporting this papers findings and therefore results cannot be ruled out. Our small sample of great apes and the possibility of ouliers in the data leave room for further investigation.

Overall

A remarkable homogeneity is present in the relative size of many of the sectors of the hominoid brain. Humans and great apes overlap in relative size of PPC, IPL and SPL through whole, left and right hemispheres, a finding that supports previous work on the volume of many sectors of the primate brain (Finlay & Darlington, 1995). Nonetheless, inter-specific and intra-specific variations exist in certain areas of the brain. Bonobos have relatively large PPC’s and IPL’s when compared to the rest of the hominoids. However, the relative size of the left IPL is larger in humans compared to any other primate sampled, apart from the bonobos. This is a positive finding regarding the left IPL area in humans and may indicate evolutionary advances in humans. EQ values were greatest among humans, followed by capuchins (see table 6). Gorilla’s indicated the lowest EQ values. These finding support research by Martin (1980) on EQ values among primates, opening up discussion on the

Evolution of the PPC 35

accuracy of EQ values based on Jerison’s (1973) research. This research has been debated in the past and other factors cited to account for overall growth in primate brains, such as social skills, genetic predisposition and diet (Gibson, 2001). This paper adds insight to this controversial area. As well as issues regarding other aspects of evolutionary growth such as allometric and isometric trends, this study applied quantative techniques which can be used to reproduce its findings in other studies. Comparisons between humans, great apes and old and new world monkeys, allowing for more thorough investigations to be conducted than in many previous investigations, many of which commonly only use one or two samples (e.g. Zilles et al, 2001).

Support from previous research

With the increases in functional imaging, the human PPC has received considerable attention (Kass et al, 2001), through PET studies (e.g. Faillenot, Toni, Decety, Gregoire & Jeannerod, 1997; Rizzolatti et al, 1996), and in more recent fMRI studies (Astafiev et al, 2004; Anderson & Goodale, 2003). Most fMRI studies however, have focused on cognitive tasks, passive sensory stimulation and simple discrimination tasks (e.g. Claeys et al, 2004; Shikata et al; 2001). This array of research has indicated the PPC in a number of cognitive abilities including planning, spatial attention, memory and even language (Kass et al, 2001). Again, few studies have investigated the evolution of the PPC across multiple primate species. This provides a greater estimate for within species variance and facilitates tests of statistical significant, affording more reliable findings.

From previous investigations, many researchers support the idea of a mosaic structure (Panda et al, 1982; Barton & Harvey, 2000; Balsters et al, 2011) and share assumptions that the evolution of the brain (or brain parts) is not a consequence of external selection pressures but

Evolution of the PPC 36

rather, a consequence of internal biological and psychological growth processes (Reader & Laland, 2001). If we consider the IPL, this area has shown to hold significantly advanced abilities, specifically in advanced tool use, yet these results were not repeated in our study. One explanation may be that within the PPC’s increasingly specialist functions are arising related to advanced species-specific behaviours. These functions may awaken in the PPC; specifically the left IPL, but rather than expanding in volume within the PPC itself, the brains vast interconnections and sophisticated support systems may have afforded the extent of the evolution to vary between components of the system (Reader & Laland, 2001).

Also, previous research by Ramnani (2006) suggest that the increasingly flexible decision making and problem solving abilities which coincide with the expansion of the prefrontal cortex, would be severely limited without the corresponding expansion of support systems. These systems could implement and store these routinely used solutions as cognitive skills. Therefore it is possible that similar expansion may have occurred within the PPC and IPL due to its connections with inputs from the motor cortex, somatosensory cortex and areas involved in vision, planning, movement and hand manipulation (Kass et al, 2011). Original functions regarding the use of tools for example, many have arisen in the IPL area, but due to connections and expansions from other areas of the cortex, broadened its cortical connection encompassing other cortical areas when activated. In turn, due to the brains remarkable ability to store and recall newly learned processes (Rizzolatti, 1996) these connections would be embedded in our neural network for future recall. This idea is supported by previous research (Chaney & Warren, 1997) indicating how substantial changes occur in the lowest neocortical processing areas and these changes can profoundly alter the pattern of neuronal activation in response to experience.

Evolution of the PPC 37

The functional organisation of the PPC has been extensively mapped during the past three decades in both humans and monkeys (Grefkes & Fink, 2005). Previous studies demonstrate that the PPC contains numerous sets of different neurons, each concerned with specific tasks including reaching, grasping, eye movements and goal directed arm and eye movements (Grefkes & Fink, 2005).. Numerous neuroimaging studies provide support for the role of the PPC in neurological deficits such as neglect syndrome, forms of apraxia and other visio-motor co-ordination problems (Marshall & Fink, 2001). However, when examining differences between species, the functional arrangement of these defined areas is not entirely equivalent (Grefkes & Fink, 2005). The interspecies differences in the functional organisation of the IPL are paralleled by structural differences in the anatomy of the intraparietal region. Namely the IPS in humans; specifically the left anterior supramarginal gyrus (aSMG), which exhibits an evolved specialisation related to tool use (Peeters et al, 2009). It is not currently understood if this functional specialization is unique to humans as investigations have only been preformed between humans and macaque monkeys and not great apes (Peeters et al, 2009).

Conclusion

This research uses modern techniques and reproducible data across a range of species in a consistent manner which builds on previous attempts to quantify aspects of the PPC. From this original research, data indicates that, contrary to what was proposed, the human IPL is the third largest relative volume in our species-sample. The greatest relative IPL volume is found among the great apes; specifically the bonobos and gorilla. Chimpanzees also possess a left IPL volume extremely similar to humans (see table 5). Therefore, a larger left IPL may indicate a hominidae trait, not related to humans alone. Findings should be taken as

Evolution of the PPC 38

preliminary, and supporting research on the functional and organisation of the IPL in great apes would be needed before any results can be stated as conclusive.

Questions regarding the organisation and evolution of the PPC and one of its main subdivisions, the IPL, cannot be answered effectively unless similarities and differences in the underlying circuitry in human and non-human primates can be identified. Although much data from older studies of the primate brain have been used in this manner by different researchers to address this issue, problems regarding methodologies issues of tissue samples, incomplete representation of hominoid species and small sample size make new investigations in this area imperative. This study reflects an effort to resolve such issues.

There are more similarities between species brains than there are differences (Krubitzer, 2009). Yet humans are fundamentally different. Human brains have undergone enormous expansion through evolution and cortical asymmetries have emerged which allow particular tasks to be processed intra hemispherically (Corbalis, 2007). Human brains have more cortical fields, cortical fields have more neurons and specific cortical fields are associated with unique behavioural specializations such as language (Krubitzer, 2009). Humans are known also to have unique and varied types of neurons (Krubitzer, 2009) and several features of gene types have been characterised as being uniquely humans and these are known to be involved in brain development (Krubitzer, 2009). So in one sense, this will make humans unique, however, all species are unique in this manner. The difficulty lies in figuring out how these varied specializations observed at all levels of organisation make us uniquely human.

Evolution of the PPC 39

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Evolution of the PPC 55

Appendix

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Table 3: Data characteristics of samples used.

*Some data was unavailable at the time of analysis

Evolution of the PPC 56

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Table 4: mean, and min and max range of volumes of ROI among species sampled

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Table 5. Relative values of ROI investigated in all species

Evolution of the PPC 58

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Table 5(a): Means and SD from MANOVA

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Table 5(b): Main MANOVA findings

Evolution of the PPC 59

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Table 6 containing EQ values, and residuals, Log actual and expected values with 95% confidence interval