Supplementary Material: Reducing the Neural Search Space for Hominid

Cognition: What Distinguishes Human and Great Ape Brains from those of

Small Apes?

1.0 Method

See Main Text (Method Section).

2.0 Results

Below we offer full results in terms of (1) number of studies used, and (2)

differences (see Supplementary Tables 1 and 2 for the data used in these analyses).

We first consider the whole brain before addressing subdivisions within the cerebral

hemispheres, and internal organization features that have been investigated in relation

to each of these subdivisions. We then consider potential interspecies differences

between the left and right sides of the brain. For the sake of brevity we only report (i)

relative and EQ results (absolute results are, with a few exceptions, larger in hominids

compared to hylobatids)1; and (ii) the observed differences between hominids and

hylobatids (note that many brain characteristics on current evidence are highly

similar; see Figure 3 and Supplementary Table 2 for full details of all comparisons).

2.1 Whole Brain

We found 10 studies involving 96 hominids and 13 hylobatids that reported

the absolute size of the brain (see Figure 3(i); de Sousa, et al., 2010; de Sousa, et al.,

2009; MacLeod, Zilles, Schleicher, Rilling, & Gibson, 2003; Rilling & Insel, 1999;

1 There were also a number of instances when EQ comparisons were inconclusive based upon violation of normality assumptions (e.g., total brain size based upon anthropoid body size). For the sake of brevity we only report EQ differences that did not involve any such violations.

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Rilling & Seligman, 2002; Semendeferi, Armstrong, Schleicher, Zilles, & Van

Hoesen, 1998, 2001; Semendeferi & Damasio, 2000; Sherwood, et al., 2007;

Sherwood, et al., 2006). Hylobatids generally possess a larger brain than

hominids (excluding humans)2 as a percentage of their total body size (de Sousa,

et al., 2009; Rilling & Insel, 1999).

2.2 Cerebral Hemispheres

We found four studies involving 55 hominids and seven hylobatids (see Figure

3(ii); Barger, Stefanacci, & Semendeferi, 2007; Schoenemann, Sheehan, & Glotzer,

2005; Semendeferi & Damasio, 2000; Semendeferi, Damasio, Frank, & Van Hoesen,

1997). No EQ values are provided due to the absence of recorded body weights from

any of these studies detailing the cerebral hemispheres.

2.3 Gray and White Matter

Gray matter receives, integrates, and produces neural information (see

Figure 3(iii-iv)). We found four studies providing gray matter data involving 48

hominids and five hylobatids (see Figure 3(iii-iv); de Sousa, et al., 2010; de Sousa, et

al., 2009; Rilling & Insel, 1999; Schoenemann, Sheehan, et al., 2005). Hylobatids

were generally found to have a larger amount of total gray matter than

hominids (excluding humans) when considered as a percentage of the cerebral

hemispheres (Schoenemann, Sheehan, et al., 2005).

2 We excluded a species from analysis if they were deemed to be unduly influencing the significance of results (i.e., they were an outlier and/or violating normality assumptions and this lead to differing results depending upon whether they were included or not). Contrast this to when we state ‘but not’; what we mean in such instances is that despite the species in question not following the trend indicated by other hominids, their inclusion or exclusion did not alter statistical findings (see Supplementary Table 2 for details of such values).

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White matter consists of myelinated axons and allows for the efficient

transfer of information between gray matter structures (see Figure 3(v)). The

amount of white matter, therefore, is a proxy indicating the degree of

connectivity within the brain. White matter can be further differentiated into two

main types. Gyral white matter immediately underlies the neocortex and is

mostly comprised of projection fibres linking neighbouring cortical regions

within the same hemisphere (Schenker, Desgouttes, & Semendeferi, 2005). Core

white matter is the remaining white matter largely consisting of long projection

fibres to other cortical regions and sub-cortical structures (Schenker, et al.,

2005). It is therefore possible to infer whether brains predominantly consist of

connections involving regions that are located either in close or distant

proximity to one another.

Our white matter analyses are based upon two studies involving 34

hominids and four hylobatids (Rilling & Insel, 1999; Schoenemann, Sheehan, et

al., 2005). There are conflicting results involving the percentage of white matter

as a proportion of the cerebral hemispheres. Schoenemann, Sheehan, et al.’s

(2005) data suggest hominids have more white matter than hylobatids only

when humans are excluded, while Rilling and Insel’s data suggests all hominids

have more white matter.3 The most likely reason for this discrepancy involves

measuring different white matter areas. Rilling and Insel only measured the

white matter immediately underlying the cerebral cortex, whilst Schoenemann,

Sheehan, et al. included white matter structures associated with both the

cerebral cortex and the internal capsule (i.e., a large sub-cortical white matter

structure sharing connections with the cerebral cortex, thalamus, and brain

3 Although Rilling and Insel’s white matter measure appears to be similar to what we have defined as gyral white matter, we are unsure whether this is actually the case.

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stem). This latter measure indicates that hominids generally have a greater

capacity for transferring neural information than hylobatids.

EQ values involving white matter are inconclusive (Rilling & Insel, 1999). An

EQ based upon anthropoid brain size does suggest that there is no difference in the

white matter immediately underlying the cerebral cortex. However, this is

questionable as it involves regressing a large portion of a variable onto itself. We

attempted to overcome this in separate analyses using both non-white matter and gray

matter, yet violations of normality occurred in both instances. As for gyral or core

white matter, only the frontal and temporal lobes have been investigated

amongst hominoids, both of which will be discussed below.

2.4 Gyrification

Another feature reflecting internal brain organization is the gyrification

index, being a proxy for the degree of neocortical folding within the cerebral

hemispheres. This is measured by obtaining the ratio between the length of the

total and superficially exposed neocortical surfaces (Rilling & Insel, 1999; Zilles,

Armstrong, Moser, Schleicher, & Stephan, 1989). Whilst larger brains tend to

have more gyrification, it is not currently known how gyrification occurs.

Richman and colleagues (1975) suggest that gyrification is due to an increase of

the outer (i.e., supragranular) layers of the neocortex relative to the inner (i.e.,

infragranular) layers. These outer layers mainly project to other cortical regions

while the inner layers project to sub-cortical layers. Therefore, according to

Richman, an increased gyrification index indicates either increased intracortical

connections or reduced descending projections to sub-cortical structures.

Alternatively, van Essen (1997) proposes that gyri are formed via the tension

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produced from axons in strongly connected regions, whilst sulci are due to the

absence of axonal tension between weakly connected regions. Increased

gyrification thus allows two strongly interrelated regions to maintain their

proximity whilst minimalizing the need for increased white matter.

We found one study including 22 hominids and four hylobatids (Rilling &

Insel, 1999). Hominids have a higher absolute level of gyrification than hylobatids

(Rilling & Insel, 1999). Assuming Richman is correct, compared to hylobatids

hominids may have either more connections with other cortical regions, or less

sub-cortical connections. If van Essen is correct, hominids may have more

connections involving interrelated regions.4

2.5 Frontal Lobes

The frontal lobes are associated with motor production and several

executive cognitive functions (see below). The frontal lobes can be subdivided

into a number of sections (e.g., motor cortex, prefrontal cortex, dorsal regions,

etc; see Figure 3(vii-xxii)), each of which will be considered after addressing the

frontal lobes as a whole. We found four studies including 32 hominids and five

hylobatids (Schenker, et al., 2005; Semendeferi & Damasio, 2000; Semendeferi, et al.,

1997; Semendeferi, Lu, Schenker, & Damasio, 2002). In terms of volume, hominids

possess larger relative values for both the frontal lobes as a percentage of the cerebral

hemispheres, and the frontal cortex as a percentage of the cerebral cortex

(Semendeferi & Damasio, 2000; Semendeferi, et al., 1997). The percentage of whole

4 A related feature to gyrification is cortical sulcal patterns. Despite not having access to the original source, we note a claim that hominids, compared to hylobatids, have sulci characterised by an increased depth, length, complexity in shape, and branch number (Connolly, 1950; cited in MacLeod, 2004).

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brain white matter that is frontal white matter is not reported because the total white

matter values needed to calculate this value were not provided.

We also considered gyral and core white matter as a proportion of the total

amount of frontal white matter (Schenker, et al., 2005; Semendeferi, et al., 1997):

hylobatids have more gyral white matter, indicating better information transfer

within the frontal lobes, and hominids have more core white matter indicating

better information transfer to sub-cortical structures and/or non-frontal regions.

These results involving core white matter should be interpreted with caution,

however, because Schenker and colleagues included portions of the amygdala

and thalamus within their measurement of frontal core white matter.

2.6 Primary Motor and Prefrontal Areas

The primary motor cortex underlies the voluntary initiation of body

movements (Ward, 2006). We found one study on the primary motor cortex

including 25 hominids and four hylobatids, with only the relative values as a

percentage of the cerebral cortex being presented (Semendeferi, et al., 2002); no

difference was reported between hominids and hylobatids.5

The prefrontal lobes have been implicated in numerous executive

cognitive functions (see below; Figure 3(xii-xiv). Only one study involving 28

hominids and two hylobatids has compared both gray and white matter

prefrontal structures (Schoenemann, Sheehan, et al., 2005). Hominids overall (but

not P. paniscus) have a higher proportion of prefrontal gray matter relative to total

cerebral gray matter. Whist a violation of normality occurred for a prefrontal gray

matter EQ based upon anthropoid non-prefrontal gray matter, hylobatids have a

5 As no individual or group mean values were provided by Semendeferi, et al. (2002) we have not included these in either Supplementary Tables.

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higher EQ value for prefrontal gray matter based upon the prefrontal white matter of

anthropoids. When using prefrontal gray matter hominids were found to have higher

EQ values for prefrontal white matter than hylobatids. However, Schoenemann,

Sheehan, et al.’s (2005) findings should be treated with caution because the

prefrontal area measured is not consistent with its cytoarchitectonic definition

(i.e., the area of frontal cortex containing a clearly distinguishable granular layer;

Elston & Garey, 2009). Rather, they adopted a proxy allowing for MRI

measurements across species: the area of the frontal lobes anterior to the genu

of the corpus callosum. This proxy results in an underestimation of the

prefrontal lobes that increases as one progresses taxonomically from monkeys to

humans, thus making it likely that hominid prefrontal values are being

underestimated in a more substantial manner than the hylobatids (Sherwood, et

al., 2005; but see Schoenemann, Glotzer, & Sheehan, 2005).

Another prefrontal study involving hominoids, but restricted to the

prefrontal cortex, is that of Semendeferi and colleagues (2002): this included 25

hominids and four hylobatids, with only the relative values as a percentage of the

cerebral cortex being published.6 Unlike Schoenemann, Semendeferi found all

hominids have more prefrontal cortex as a percentage of total cerebral gray

matter. The likely reason for this discrepancy is that Semendeferi measured an

area of the frontal lobes including the prefrontal cortex, the premotor cortex, and

some limbic cortices. This proxy captures the entire prefrontal cortex, yet

possible differences in the premotor and limbic cortices may still be confounding

results.7

6 See previous footnote.7 We do find hominids have a relatively larger orbitofrontal region (which contains limbic cortex; section 2.10 below), but conversely, hylobatids have a relatively larger amygdaloid complex (section 2.19.2 below).

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2.7 Brodmann’s Area 10

An important subsection of the prefrontal lobes is Brodmann’s Area 10

(BA 10; see Figure 3(xv); Semendeferi, et al., 2001). In humans this region is

implicated in episodic and working memories, planning future actions,

undertaking initiatives, facilitating the extraction of meaning from ongoing

experience, organizing mental contents which control creative thinking and

language, and sustained attention (Allman, Hakeem, & Watson, 2002;

Semendeferi, et al., 2001). Based upon one comparison including 12 hominids and a

single hylobatid (Semendeferi, et al., 2001), BA 10 is larger in hominids as a

percentage of the total cerebral hemispheres. Moreover, in hominids BA 10 is

usually equivalent to most of the frontal pole. However, hylobatids have a frontal

pole comprising of two anatomically distinct regions, a dorsal and a orbital

region, with only the latter assigned as BA 10.8

There are also microanatomical differences within this region, each of

which is indicative of differences in internal organization. Firstly, the lower

neuronal cell density for hominids suggests that they possess the general

capacity for more connections within this region. Similarly, hominids (but not P.

pygmaeus) possess a lower grey level index (i.e., the percentage of grey cell

8 Semendeferi and colleagues (2001) note: “In the line leading to gibbons [in relation to Old World monkeys], the topographic location and probably the extent of area 10 did not change appreciably. In Asian and African large bodied hominoids, area 10 came to occupy the entire frontal pole and is now present in orang-utans, chimpanzees, bonobos, and humans. The preliminary findings on the gorilla suggest that in the line leading to this great ape, area 10 was either selectively reorganized or shifted to a different location within the rostral prefrontal cortices” (p. 239). However, as with the gibbon, there is only one gorilla included in this analysis, raising concerns about generalizability of the data.

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bodies) indicating an increased capacity for more neural connections.9 A more

specific finding is that hominids (but not P. pygmaeus) have a lower grey level

index within the infragranular layer. This means, tentatively at least, that

hominids have more connections with distal cortical and/or sub-cortical regions,

but also, more feedback connections to BA 10 itself. In contrast, hylobatids have

a larger granular layer as a proportion of the combined neocortical layers within

BA 10. This suggests hylobatids receive more neural connections within and

between the cortical columns located within BA 10 itself.

2.8 Brodmann’s Area 9L

Brodmann’s Area 9L (BA 9L) is another prefrontal area which in humans

has been associated with working memory (see Figure 3(xvi); Sherwood, et al.,

2006). Whilst there is no data on the size of this region, one study involving 13

hominids and a single hylobatid has provided values for the density of neurons

and glial cells within the supragranular layers (Sherwood, et al., 2006).10 Neural

density is higher for hominids compared to hylobatids, suggesting the latter have

an increased capacity for more proximal connections within the supragranular

layers of BA 9L. No differences in glial density were observed in terms of

absolute or EQ values based upon anthropoid BA 9L neuronal density. It may

therefore be tentatively inferred that all hominoids have similar metabolic

9 The relationship between gray level index and neuronal density is such that variations in the gray level index within a species are primarily due to neuronal density. The emphasis within the gray level index is on neurons because glial and endothelial cells constitute a small percentage of the cortex, and furthermore the density of glial cells remains constant between cortical layers (Semendeferi, et al., 1998). 10 Keep in mind it is unlikely that glial cell density varies throughout the various layers of neocortex (Semendeferi, et al., 1998).

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demands associated with this region, as glial cells play a crucial role in supplying

neurons with the energy they require (Sherwood, et al., 2006).

2.9 Dorsal Frontal Lobes

The dorsal region includes Broca’s area (i.e., BA 44 and BA 45) along with

most of the premotor and motor cortices (see Figure 3(xvii-xix)). In addition to

its involvement in language and motor production, the dorsal region is

associated with perception, response selection, working memory, and problem

solving (Schenker, et al., 2005). We found two studies including 31 hominids and

four hylobatids (Schenker, et al., 2005; Semendeferi, et al., 1997). Conflicting results

exist for the volume of the dorsal sector as a percentage of the frontal lobes.

Based upon data provided by Semendeferi and colleagues (1997), which include

only one hylobatid, hominids appear to have the larger dorsal sector. However,

this data set produced a violation of normality. Based upon data involving three

specimens, hylobatids have the larger dorsal sector after P. pygmaeus is

excluded (Schenker, et al., 2005).11 As a percentage of the total frontal cortex,

hominids (but not P. paniscus) generally have more dorsal cortex (Schenker, et

al., 2005). Hylobatids have more dorsal gyral white matter when considered as a

percentage of total frontal gyral white matter (Schenker, et al., 2005).

2.10 Orbital Frontal Lobes

The orbital region is located along the bottom of the frontal lobes (see

Figure 3(xx-xxii). Unlike the dorsal and mesial regions, the orbital region appears

11 We are presently at a loss as to why there is such a discrepancy in the relative values associated with these two studies. Given that they appear to use similar segmentation procedures, we can do no better than assume that intraspecies variation may be primarily responsible.

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to have minimal involvement in executive cognitive functions. Documented

human cases involving damage to this area report minor impairments to

language, attention, and memory (Damasio, 1994; Schenker, et al., 2005; Stuss &

Benson, 2005). This region does appear to have a substantial role in the

emotional and social processes typically associated with complex social groups

(e.g., learning social rules; see section 2.11; Schenker, et al., 2005).

We found two studies including 31 hominids and four hylobatids (Schenker, et

al., 2005; Semendeferi, et al., 1997). There is conflicting data for absolute values of

the orbital sector. Semendeferi and colleagues’ (1997) study involving one

hylobatid indicates that there is no difference, while the larger data set from

Schenker and colleagues (2005) suggests that hominids are larger. As a

percentage of the frontal lobes, we again found conflicting data. Semendeferi, et

al. (1997) indicates that there is no difference, yet hylobatids are larger

according to the data from Schenker and colleagues (2005). Hylobatids do have a

higher percentage of orbital cortex in relation to the frontal cortex, whilst

hominids (excluding P. pygmaeus) generally have more orbital gyral white

matter as a percentage of total frontal gyral white matter (Schenker, et al., 2005).

2.11 Area 13

A specific part of the orbital region, known as Area 13 (see Figure

3(xxiii), is predominantly involved in emotional and social processing.

Destruction of Area 13 in macaques leads to impairments in their construction

and maintenance of social bonds. This is exemplified by their disinhibition of

inappropriate emotional responses (e.g., showing hostility when non-threat

stimuli are presented), and alternatively, their inhibition of appropriate

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emotional responses (e.g., showing no hostility when presented with threatening

stimuli; Semendeferi, et al., 1998). The contribution of Area 13 to emotional

processing is also reflected in the extensive connections it has with other

emotional regions including the amygdala, ventral striatum, and the nucleus

basalis of Meynert, along with the insula, temporal polar, and parahippocampal

cortices.

We found one study for Area 13 involving 17 hominids and two hylobatids

(Semendeferi, et al., 1998). Hominids typically have Area 13 positioned in the

caudal regions of the medial orbital and posterior orbital gyri, whereas

hylobatids appear to have Area 13 confined within the caudal part of the medial

orbital gyrus.12 As for the internal organization of Area 13, hominids (but not P.

pygmaeus) do possess wider infragranular layers as a proportion of the

combined layers within this region, suggesting they possess a higher percentage

of long range and/or sub-cortical projections, along with more feedback

connections within Area 13 itself. Hominids possess higher gray level index

values for Area 13 as a whole, and for both the supra and infragranular layers

within this area. This suggests that Area 13 within hylobatids may generally have

the potential for more neural connections to both distal and proximal regions.

2.12 Mesial Frontal Lobes

12 We acknowledge that Area 13 within the orang-utan, whilst sharing many similarities with the great apes, also possesses unique characteristics not evident in the other great apes. These include: (1) a more anterior position in the mesial orbital and posterior orbital gyri; (2) having cortical features more typical of prefrontal association cortex as opposed to limbic cortex; (3) taking up a larger portion of the orbitofrontal sector (although this is probably due to the orang-utan possessing a smaller orbital frontal region in comparison to the other great apes). Given the role of Area 13 in social behaviour, these features may contribute to the lower amount of social interaction observed with the orang-utan relative to that seen in other hominoids (Semendeferi, et al., 1998).

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The mesial (i.e., midline) frontal region includes some premotor and

primary motor cortices, along with the anterior cingulate gyrus (see Figure

3(xxiv-xxvi)). This region, especially the anterior cingulate gyrus, has been

implicated in attention management, decision making, self control, social

awareness, empathy, theory of mind, and emotional behaviors (Critchley,

Mathias, & Dolan, 2001; Lane, et al., 1998; O'Doherty, Critchley, Deichmann, &

Dolan, 2003; Posner & Rothbart, 1998; Schenker, et al., 2005; Watson & Allman,

2007). We found two studies including 31 hominids and four hylobatids (Schenker, et

al., 2005; Semendeferi, et al., 1997). No differences in either relative size or EQs were

found for any feature of this region (i.e., total sector, gray matter, total white matter,

and gyral white matter).

2.13 Insula Lobes

The insula lobes are buried within the junction between the posterior

frontal and anterior temporal lobes (see Figure 3(xxvii). Predominantly studied

using humans, this region is implicated in autonomic responses, olfaction, taste,

attention, decision making, perceiving and experiencing emotional expressions,

judging the trustworthiness of others, and body perception (Fabbri-Destro &

Rizzolatti, 2008; Ward, 2006; Watson & Allman, 2007). One recent review has

even speculated that this region may contribute to human awareness (Craig,

2009). We found one study including 25 hominids and four hylobatids (Semendeferi

& Damasio, 2000). Hominids have larger insula lobes as a percentage of the

cerebral hemispheres (Semendeferi & Damasio, 2000).

2.14 Temporal Lobes

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The temporal lobes are involved in several capacities generally associated

with audition, vocalization, vision, memory and emotion (see Figure 3(xxviii-

xxxiii); Rilling & Seligman, 2002). We found three studies addressing the temporal

lobes including 32 hominids and four hylobatids (see Figure 3(xxviii-xxxiii); Rilling

& Seligman, 2002; Schenker, et al., 2005; Semendeferi & Damasio, 2000). Only one

study provided data on gyral and core white matter (Schenker, et al., 2005), and one

addressed the superior temporal gyrus and temporal lobe gyrification (Rilling &

Seligman, 2002).

As a percentage of the brain and cerebral hemispheres hylobatids have larger

temporal lobes (Rilling & Seligman, 2002; Semendeferi & Damasio, 2000). No

relative gray matter values are reported due to the absence of the required data within

a single study (i.e., both temporal gray matter and total cerebral gray matter).

Hylobatids have a larger amount of temporal white matter as a percentage of

total brain white matter, whilst hominids have more white matter as a

proportion of the temporal lobes (Rilling & Seligman, 2002; Schenker, et al.,

2005). As a percentage of temporal white matter, hylobatids have more gyral white

matter whilst hominids have more core white matter (Schenker, et al., 2005). The

absolute gyrification index for the whole temporal lobe is higher in hominids

(Rilling & Seligman, 2002). Finally, the volume of the superior temporal gyri, a

region predominantly implicated in species-specific auditory processing, was

found to be a higher percentage of the whole brain in hylobatids (Rilling &

Seligman, 2002).

2.15 Parieto-occipital Lobes

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The parieto-occipital region refers to the combined parietal and occipital

lobes; these lobes predominantly perform somatosensory and visual processing

respectively, yet both also contribute to spatial awareness and attention (see

Figure 3(xxxiv); Ward, 2006).13 We found one study providing data for the

combined parieto-occipital lobes, involving 25 hominids and four hylobatids

(Semendeferi & Damasio, 2000). As a percentage of the cerebral hemispheres,

hylobatids generally have larger parieto-occipital lobes than hominids (excluding

G. gorilla).

2.16 Area V1

Area V1 is the primary visual cortex, which predominantly processes

visual information allowing for the initial detection of edges, orientation, color,

and luminance (see Figure 3(xxxv); Ward, 2006). We found three studies

including 35 hominids and four hylobatids (see Figure 3(xxxv); de Sousa, et al.,

2010; de Sousa, et al., 2009; Sherwood, et al., 2007). Hylobatids have higher

relative values for V1 gray matter when measured either as a proportion of the

total brain or neocortex (de Sousa, et al., 2010; de Sousa, et al., 2009). No values

for V1 white matter were provided by the original sources.14 GLI values for the

total layers of V1 neocortex were generally lower for hominids as hylobatids

have higher values for both the supragranular and infragranular layers (de

Sousa, et al., 2009). These GLI values indicate that hominids may have a greater

capacity than hylobatids for more neuronal connections from V1 to both

13 Semendeferi and Damasio’s (2000) combination of the parietal and occipital lobes is due to the absence of a common external marker that reliably distinguishes these regions amongst all species.14 Unlike other regions of neocortex, layer IV of area V1 has four distinct sub-layers. Here we report the combined granular layer to be consistent with other regions discussed within this paper.

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proximal and distal brain regions, along with increased feedback connections

within V1 itself.

Another microfeature of this area involves inhibitory interneurons (i.e.,

neurons which mediate processing between afferent and efferent neurons within

any given neural pathway; Rosenzweig, Breedlove, & Leiman, 2002). Knowing

the proportion of inhibitory interneuron sub-types allows one to determine

whether interspecies differences exist in how neural processing occurs within

any given area (Sherwood, et al., 2007). For example, double bouquet and bipolar

neurons may predominantly function by vertically inhibiting neural activity

throughout the various layers within the mini-column they originate (mini-

columns are vertically organised groups of about 80-100 neurons located within

the cerebral cortex, and are considered to be one of the most basic modular

components involved in cognitive processing);15 this in turn may allow for the

synchronization of activity of neurons within any single mini-column (Sherwood,

et al., 2007). Interneurons which function by inhibiting other neurons within the

same layer of cortex, but in different mini-columns, include large basket and

chandelier cells; these cells may ultimately determine the size of the receptive

fields of pyramidal cells within and surrounding any given mini-column

(Sherwood, et al., 2007). Based on one study involving eight hominids and one

hylobatid (Sherwood, et al., 2007), hominids have more double bouquet and

bipolar cells reactive to the immunohistochemical agent calretinin, regardless of

whether measured absolutely, as a percentage of V1 total supragranular density,

or as an EQ based upon anthropoid supragranular density. Hominids, therefore,

may have an increased capacity for the vertical inhibition of cells within any

15 For discussion concerning potential interspecies differences involving mini-columns see papers by Buxhoeveden and colleagues (2002; 2001).

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given mini-column found within V1. As for basket and chandelier cells,

hylobatids were found to have more of these within the supragranular layers of

V1, both absolutely and as a proportion of total V1 supragranular density. These

findings indicate that hylobatids may have more potential for the lateral

inhibition of pyramidal cells within the supragranular layers of V1, which in turn

may result in differences involving the types of receptive fields characterizing

this region when compared to hominids.

2.17 Area V2

In addition to the features characteristic of V1, area V2 also processes

information leading to the recognition of form, as indicated by cells within this

area being sensitive to illusory contours (see Figure 3(xxxvi); Rosenzweig, et al.,

2002). We found three studies including 35 hominids and four hylobatids (see

Figure 3(xxxvi); de Sousa, et al., 2010; de Sousa, et al., 2009; Sherwood, et al.,

2007). No absolute values were provided for the size of this area, which

subsequently disallowed analyses involving relative and EQ values. As a

percentage of the combined layers the width of the supragranular layers was

larger for hominids, suggesting more connections with proximal cortical regions.

The infragranular layers were larger for hylobatids (but not P. troglodytes),

suggesting more connections with distal regions and more feedback connections

within V2 itself (de Sousa, et al., 2009).16 The supragranular layers have a higher

neuronal density for hylobatids when measured absolutely, but not when

predicted upon anthropoid brain size (Sherwood, et al., 2007). Hylobatids have

16 Unlike other regions of neocortex, area V2 layer III has numerous sub-layers, but we simply report the supragranular layers to be consistent with other areas within this paper.

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higher GLI values for the supragranular, granular, and infragranular layers (de

Sousa, et al., 2009). These microfeatures indicate that hominids have more

potential for neuronal connections within and beyond area V2. As for

interneuron sub-types, hominids had more cells reactive to calbindin D-28 when

measured using an EQ based upon anthropoid V2 supragranular density. This

suggests that compared to hylobatids, hominids may have an increased capacity

for inhibiting cells within mini-columns found in V2.

2.18 Area VP

Area Ventral Posterior (VP), also known as V3 ventral and/or V3a,

contributes to visual motion processing in humans and monkeys (see Figure

3(xxxvii); Moutoussis, Keliris, Kourtzi, & Logothetis, 2005). There is only one

study including seven hominids and one hylobatid (de Sousa, et al., 2009). As a

percentage of the combined layers hominids (excluding humans) have a wider

granular layer, whilst hylobatids have relatively wider infragranular layers. This

suggests that hominids generally have a higher percentage of connections within

area VP than hylobatids, whilst hylobatids have more distal and feedback

connections. Hylobatids have higher GLI values for the supragranular, granular,

and infragranular layers of VP neocortex, indicating that hominids may generally

have a greater capacity for more neuronal connections throughout the various

layers of VP.

2.19.0 Sub-cortical and Brainstem Structures

Compared to the small amount of studies meeting our criteria for cortical

structures, there has been even less research addressing the potential

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similarities and differences involving sub-cortical structures. Below we discuss

the lateral geniculate nucleus, amygdaloid complex, and the orofacial system.

2.19.1 The Lateral Geniculate Nucleus

The lateral geniculate nucleus, located within the thalamus, serves as the

major intermediate area of the visual system: it relays input from retinal

ganglion cells to V1, and to a lesser extent area V5 (i.e., which is primarily

responsible for processing visual motion; see Figure 3(xxxviii); de Sousa, et al.,

2010; Rosenzweig, et al., 2002). We found two studies involving 27 hominids and

three hylobatids (de Sousa, et al., 2010; de Sousa, et al., 2009). Hylobatids have a

larger lateral geniculate nucleus as a percentage of the total brain (de Sousa, et

al., 2010).

2.19.2 The Amygdaloid Complex

The anterior region of the medial temporal lobe contains the amygdaloid

complex (see Figure 3(xxxix-xliii)), which is a major structure associated with

emotion, attention and perception, learning, memory (both implicit and explicit),

and social interaction (Barger, et al., 2007; Phelps & LeDoux, 2005). Most

research on this region has involved using rats to learn the mechanisms

associated with fear conditioning (Phelps & LeDoux, 2005). Macaque single cell

studies implicate that the amygdaloid complex responds to images of faces and

the social approaches of other monkeys, whilst a variety of human studies

suggest it is involved with gaze monitoring, processing emotional expressions,

judging people’s trustworthiness, and deciding whether to conform to other

people’s suggestions (Barger, et al., 2007).

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The amygdaloid complex can be coarsely divided into the basolateral

division and non-basolateral division. While the non-basolateral division is

implicated in ‘survival’ processes by virtue of its association with the brain stem

and olfactory nuclei, it is the basolateral division that appears to be underlying

important abilities that contribute to effectively processing social and emotional

information (e.g., associative learning, pairing affective values with sensory

input, etc; Barger, et al., 2007). Indeed, despite the absence of any relationship

between the whole amygdaloid complex and measures of sociality (Joffe &

Dunbar, 1997), increases in the basolateral division are associated with

increases in primate social group size (Barton, Aggleton, & Grenyer, 2003).17

Furthermore, the role of the basolateral division in social and emotional

processing is reflected in the connections that each of its three nuclei have with

other cortical regions (which are also implicated in social and emotional

processing): (1) the lateral nuclei receives sensory input from the temporal lobe;

(2) the basal nuclei receives input from the orbitofrontal cortex; and (3) the

accessory basal nuclei receives input from the orbitofrontal cortex, BA 10, and

the superior temporal sulcus.18

We found one study including 10 hominids and two hylobatids (one being

H. lar and the other being H. concolour) (Barger, et al., 2007). As a percentage of

17 It should be noted that the reported relationship by Barton and Aggleton involved the corticobasolateral division of the amygdaloid complex, which is mainly comprised of the basolateral division. We have referred to this region as the basolateral division to be consistent with the discussion that follows involving Barger, et al.’s data. 18 As for the possible network involving these regions, it’s been hypothesized that sensory information provided from the temporal lobe is categorized by the lateral nuclei, after which the basal nuclei integrates and evaluates this information with the input it receives from the orbitofrontal cortex concerning the social context within which the sensory information occurred. Ultimately, this evaluation allows for a context appropriate response to be generated by hypothalamic and brainstem nuclei via the basal nuclei’s connections with the central nuclei and striatum (Barger, et al., 2007).

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the cerebral hemispheres, hylobatids have both a larger amygdaloid complex and

basolateral division. Considered in relation to the amygdaloid complex, hominids

have a larger basolateral division when compared against H. concolour, but not

H. lar. Given that these species are represented by merely one specimen, this

may reflect individual rather than species differences. This nevertheless serves

to illustrate the potential limitation of having hylobatids be represented by H.

lar only (see main text Section Low numbers of subjects and species for more

discussion).

2.19.3 The Brainstem Orofacial System

The orofacial motor system is located within the medulla and is involved

in the production of respiration, feeding, vocalization, speech/communication,

and facial expression (Sherwood, et al., 2005). The orofacial muscles in this

system are separately innervated by motor neurons from three cranial nuclei

(see Figure 3(xliv-xlvi)).19 The trigeminal nuclei (i.e., cranial nerves Vmo)

provide input to muscles involved in mastication. The facial nuclei (i.e., cranial

nerves VII) supplies input for the muscles controlling facial expressions, which

are an important feature of anthropoid social communication in general

(Sherwood, et al., 2005). Finally, the hypoglossal nuclei (i.e., cranial nerves XII)

innervate muscles of the tongue that may be important for producing

vocalizations (Sherwood, et al., 2005).

Our analyses of these nuclei are all based upon data from one study of 16

hominids and three hylobatids (with the exception of gray level index values,

19 There is a fourth nucleus consisting of ambiguous motor neurons that innervate muscles of the pharynx, larynx, and esophagus. We do not discuss this structure as Sherwood and colleagues (2005) do not provide data for it.

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which included 14 hominids and two hylobatids) (Sherwood, et al., 2005). The

only observed differences with respect to either relative size or EQ involved the

facial nuclei, with hominids possessing higher values as a percentage of the

medulla. Gray level index values only differed for the trigeminal nuclei, with

hylobatids having a higher value compared to hominids, suggesting that the

latter have the potential for more connections.

2.20 Cerebellum

The cerebellum (see Figure 3(xlvii-xlix)) can be broadly divided into two

functionally distinct areas: the medial and lateral sectors. The medial sector,

consisting of the vermis and paravermis, is involved in motor performance (i.e.,

balance and co-ordination). The lateral sector, consisting of the cerebellar

hemispheres, is implicated in several cognitive abilities including the planning of

complex movements, procedural learning, visuo-spatial problem solving, the

shifting of visual attention, and language (MacLeod, et al., 2003; Rilling, 2006).

These characteristics have lead to the suggestion that the lateral sector may be

an important component in hominoid locomotion, tool making, and language

acquisition (MacLeod, et al., 2003).

We found two data sets for the cerebellum, including 55 hominids and

nine hylobatids (MacLeod, et al., 2003; Semendeferi & Damasio, 2000). Of these,

only one reported the medial and lateral cerebellar regions (MacLeod, et al.,

2003). Hylobatids have a larger medial sector as a percentage of the cerebellum,

however EQ values for the medial sector are larger for hominids based upon the

anthropoid lateral sector (MacLeod, et al., 2003). The relative value of the lateral

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sector is larger in hominids, yet based upon the anthropoid medial sector, lateral

EQ values are larger in hylobatids (MacLeod, et al., 2003).

2.21 Asymmetries

Neuroanatomical asymmetries have been identified in a number of

primates, including all apes. While the relationship between asymmetry and

function is not completely understood, studying asymmetries provides another

avenue for understanding brain organisation (Galaburda & Rosen, 2003). For

example, anatomical areas that are asymmetrical do tend to receive fewer

callosal connections, indicating that increased asymmetry results in greater

intrahemispheric connectivity (Galaburda & Rosen, 2003).

To reduce space, data for asymmetries are not provided in either Figure 3 or

Supplementary Tables 1 and 2 (although we note that very little data has been

presented for each separate hemisphere). Hominids and hylobatids appear to share a

number of anatomical asymmetries. With respect to the frontal lobes of all hominoids,

there are conflicting claims about whether the right or left frontal lobe is larger. On

the one hand Semendeferi, et al. (2001) found that the total frontal lobe (i.e., cortex

and white matter) is larger in the right hemisphere. Conversely, Schenker and

colleagues (2005) report that (1) the frontal cortex is larger in the left hemisphere, (2)

there is no asymmetry involving gyral white matter, and (3) core white matter is

larger in the right hemisphere. This potential discrepancy does require further

clarification, yet hominids and hylobatids were found to share these features in each

respective study. Asymmetries in the three major sectors within the frontal lobes also

appear to be shared. The dorsal and mesial frontal cortices appear to be larger in the

right and left hemispheres respectively (but not for H. sapiens), while there is no

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asymmetry involving the orbital sector (Schenker, et al., 2005). No gyral white matter

asymmetries appear to be present within any of these sectors (Schenker, et al., 2005).

Hominids and hylobatids also share the presence of a petalia (i.e., protrusion) within

the right prefrontal lobe (Galaburda & Rosen, 2003), however this area largely

consists of BA 10, which contains qualitative and quantitative features differentiating

hominids from hylobatids (see above section 2.7). No systematic asymmetries have

been reported involving either the volume or surface area of the temporal lobes, nor

for any gray and white matter structures within this region (Schenker, et al., 2005).

Yet there are sulcal features within the temporal lobes differentiating hominids from

hylobatids. Unlike hylobatids, hominids have a larger sylvian fissure and planum

temporale in the left compared to right hemisphere, both of which are thought to

be associated with language in humans (Hopkins, Marino, Rilling, & MacGregor,

1998; LeMay & Geschwind, 1975). However, we do note that the temporal

gyrification index is higher in the left compared to right hemisphere only for

hylobatids (Rilling & Seligman, 2002). As for the occipital lobes, all hominoids share

the presence of a petalia within the left hemisphere (Galaburda & Rosen, 2003).

Only one sub-cortical structure has published data for the right and left

hemispheres separately. The amygdaloid complex does not appear to be

systematically asymmetrical in either hominids or hylobatids, nor does there appear to

be any systematic differences for any of the nuclei making up the basolateral division

(Barger, et al., 2007). 20

As for functional asymmetries considerable evidence suggests that

hominids, with the exception of orangutans, are predominantly right handed for

bimanual object manipulations (Hopkins, et al., 2011). Whilst not tested using

20 It is important to note that Barger, et al. had orang-utan subjects in which the right hemisphere values were doubled for some aspects of the amygdaloid complex.

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the same task, hylobatids have been found to predominantly use their left hand

for a complex task - scooping water - whilst hanging from a branch using their

right hand (Morino, 2011).

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