Supplementary Material: Reducing the Neural Search Space for Hominid Cognition: What

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; 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).

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 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 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 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 EQbased upon anthropoid non-prefrontal gray matter, hylobatids have a 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]

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 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 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 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 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

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).