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. Author manuscript; available in PMC: 2020 Sep 1.
Published in final edited form as: Cortex. 2019 May 16;118:306–314. doi: 10.1016/j.cortex.2019.05.004

Investigating Individual Differences in Chimpanzee Mirror Self-Recognition and Cortical Thickness: A Vertex-Based and Region-of-Interest Analysis

William D Hopkins 1, Robert D Latzman 2, Lindsay M Mahovetz 2, Xiang Li 3, Neil Roberts 3
PMCID: PMC6697634  NIHMSID: NIHMS1531872  PMID: 31204008

Abstract

Mirror self-recognition (MSR), a recently evolved cognitive trait, is one of the most significant abilities that separate humans and great apes from more distantly related nonhuman primates. MSR may serve as the foundation for a number of related but more complex social cognitive abilities unique to humans and great apes including imitation, empathy, theory-of-mind, perspective taking and deception. However, our understanding of the neural basis of MSR in nonhuman primates remains largely unknown. The current study aimed to begin to fill this gap in the literature by investigating the neuroanatomical foundations of MSR in a sample of 67 captive chimpanzees. Vertex-based and region-of-interest analysis revealed significant differences in cortical thickness, particularly in males, in the cingulate cortex, inferior frontal gyrus and superior temporal and frontal cortex. The current study provides further evidence for the neuroanatomical foundations of mirror self-recognition abilities in chimpanzees.

Keywords: Self-recognition, Mirror self-recognition, Neuroimaging, Social cognition, chimpanzees, nonhuman primate models

First described by Gallup (1970), the ability to recognize one’s own appearance in a mirror, known as mirror self-recognition (MSR), is one of the most significant abilities that separate humans and great apes (i.e., gorillas, orangutans, chimpanzees & bonobos) from more distantly related nonhuman primates. Indeed, with respect to the order Primates, to differing degrees all the great apes show MSR without any explicit training while all non-ape species, including lesser apes, Old and New World monkeys as well as prosimians, do not (see Anderson & Gallup, 2011, 2015; Parker, Mitchell, & Boccia, 1994 for reviews). Results of this large and generally consistent body of literature suggest that MSR is a recently evolved cognitive trait and may serve as the foundation for a number of related complex social cognitive abilities (Keenan, Gallup, & Falk, 2003). According to some, MSR abilities may reflect one set of cognitive skills within a larger suite of socio-cognitive processes that may be unique to human and great apes including, for example, imitation, empathy, theory-of-mind, perspective taking and deception (Gallup, 1985; Mitchell, 1993, 1997). Developmental studies in human children support this view. For example, MSR performance in young children has been reported to correlate with the emergence of language, empathy (Bischof-Kohler, 2012), pretend play (Lewis & Ramsay, 2004; Nielsen & Dissanayake, 2004), mutual gaze/joint attention abilities (Nichols, Fox, & Mundy, 2005) and imitation (Asendorpf & Baudonniere, 1993; Asendorpf, Warkentin, & Baudonniere, 1996). Nonetheless, the exact way in which MSR abilities situate within a larger suite of socio-cognitive abilities, both developmentally and temporally (that is, upon which abilities subsequent abilities rely) is far from clear (Frith & Frith, 2005).

Regardless, much of the last half century of research on MSR in human and nonhuman primates has primarily focused on descriptive studies identifying various correlates of MSR and in which species, what patient populations, or at what age MSR develops. While these studies have provided critical descriptive information concerning this important evolutionary and developmental process, there have been exceedingly few studies that have attempted to characterize the mechanisms that underlie individual differences in MSR. Notably, among great apes, numerous studies have reported that some proportion of individuals within a sample fail the mark test (Allen & Schwartz, 2008; Ledbetter & Basen, 1982; Posada & Colell, 2007; Suarez & Gallup, 1981; Swartz & Evans, 1991). For example, in a sample of more than 100 chimpanzees, Povinelli, Rulf, Landau, and Bierschwale (1993) reported that ~ 35% of the individuals failed to show any compelling evidence of MSR. Likewise, in a sample of 73 chimpanzees, Mahovetz, Young, and Hopkins (2016) reported that 45% were judged to show no evidence of MSR abilities. What remains unclear from the existing nonhuman primate literature is why some individuals pass and some fail the mark test. Some have suggested that the high degree of individual variability in MSR performance simply reflects that lack of sensitivity of the mark test to adequately and accurately measure self-recognition abilities (Bard, Todd, Bernier, Love, & Leavens, 2006; De Veer & Van Den Bos, 1999; Heschl & Burkart, 2006). Others have suggested that characteristics such as sex, age, and rearing experience may mediate the expression of MSR abilities (Bard et al., 2006; Gallup, McClure, Hill, & Bundy, 1971; Hopkins, 2008; Lin, Bard, & Anderson, 1992).

Two recent studies have tested whether variation in genes and cortical connectivity may explain some individual differences in MSR abilities. First, Mahovetz et al. (2016) tested whether polymorphisms in the vasopressin V1a receptor gene (AVPR1A) influenced MSR and related social behaviors in response to a mirror. Mahovetz et al. (2016) did not find a significant relationship between AVPR1A polymorphism and MSR abilities; however, these authors did find that males with the DupB+/− polymorphism showed significantly higher rates of agonistic and scratching behavior (reflecting anxiety) in response to the mirror compared to DupB−/− males and both genotypes in females. In the Mahovetz et al. study, 75% of the DupB+/− males failed to show compelling evidence of MSR and they suggest that the increased agonistic and anxiety responses to their mirror reflection inhibited their abilities to engage in contingent actions with their mirrored reflection that would lead to overt expression of MSR. In a second study, Hecht, Mahovetz, Preuss, and Hopkins (2017) quantified the superior longitudinal fasciculus (SLF) white matter tract in 60 chimpanzees that were judged to reliably exhibit or not exhibit mirror self-recognition. Hecht et al. (2017) found that chimpanzees judged to exhibit MSR had increased rightward asymmetries in SLFII and SLFIII tracts and significantly more terminations in the right Broca’s area compared to individuals that were judged not to exhibit MSR.

Here, we further examined whether individual variation in MSR abilities among chimpanzees are associated with cortical thickness in certain neuroanatomical regions of the brain. In humans, research suggests specific cortical correlates of self-recognition (Devue et al., 2007; Sugiura et al., 2005) as well as associations between variation in cortical thickness and related cognitive abilities (Bertrand et al., 2018). Further, recent studies in chimpanzees have found that variation in the integrity of white matter tracts is associated with self-recognition abilities (Hecht et al., 2017) and that individual variation in general cognitive abilities are associated with region specific variation in cortical thickness (Hopkins, Li, & Roberts, in press). Because MSR arguably reflects at least some dimension of social cognition, we hypothesized that variation in MSR performance may similarly be associated with cortical thickness. Specifically, using both a vertex-based and region-of-interest methods, we tested for differences in cortical thickness between chimpanzees that showed varying MSR abilities. In humans, a number of functional imaging studies have shown that brain structures including the medial prefrontal cortex, inferior frontal gyrus, anterior cingulate cortex, and fronto-insular cortex, among others, play an important role in discriminating self from others (Kircher et al., 2001; Platek, Wathne, Tierney, & Thomson, 2008; L. Q. Uddin, Iacoboni, Lange, & Keenan, 2007). Additionally, other functional imaging studies have clearly implicated the fronto-insular cortex with more complex socio-emotional processes such as empathy and perspective taking (Brooks & Tracey, 2007; Craig, 2009; Decety, 2010; Iacoboni, 2009; Lamm & Singer, 2010; Redcay, Kleiner, & Saxe, 2012; L. Q. Uddin & Menon, 2009), socio-cognitive processes hypothesized to be linked to MSR abilities (Gallup, 1982, 1985; Sowden & Shah, 2014). Based on these findings, we hypothesized that significant differences in cortical thickness would be evident in midline brain structures in the chimpanzees. Based on the DTI finding by Hecht et al. (2017) reporting increased SLF termination in the inferior frontal gyrus of chimpanzees that pass the mark test, we further hypothesized that significant differences in cortical thickness would be found in this brain region.

Methods

Subjects

The sample consisted of 67 captive chimpanzees, including 21 males (Mage = 18.95 ± 4.85) and 46 females (Mage = 25.85 ± 12.31) ranging in age from 9 to 54 years, housed at Yerkes National Primate Research Center (YNPRC). Chimpanzees were housed in social groups ranging from two to 14 individuals. All study procedures were conducted in accordance with the Committee on the Care and Use of Laboratory Animal Resources and were approved by the local Institutional Animal Care and Use Committee.

Mirror Self Recognition Task

As described previously by Mahovetz et al (2016), each subject was temporarily singly shifted, when possible, into a non-hazardous enclosure and videotaped for a 10-min long test session. An acrylic/Plexiglas mirror measuring approximately 91.44 cm in height and 60.96 cm in width stabilized within a steel frame and base was used during testing. The mirror was placed approximately 30.48 cm away from the subject. The mirror faced away from the subject before marking to prevent early exposure. All sessions were filmed using a Canon Vixia series digital video camera with an attached wide-angle lens mounted on a tripod set-up behind and above the mirror. The camera was positioned at a downward angle to capture the subject’s behaviors while in front of the mirror.

Blue colored non-toxic food dye was used for marking subjects’ mouths and was mixed with sugar-free Kool-Aid. The food dye met all FDA safety guidelines and was rated safe as an ingestible dye for human food products. Since subjects are regularly given juice, it was assumed that subjects did not know they were being marked prior to mirror exposure. After giving the marker, the experimenter turned the mirror to face the subject. Once the subject was positioned in front of the mirror, the 10-min session began. When necessary (i.e. if the subject was hanging on the cage above the mirror), a small amount of Kool-Aid or piece of fruit was used to position the subject in front of the mirror. The experimenter left the area to reduce experimenter directed behavior during the test session. After the 10-min session, the experimenter returned and reunited the subject to their original group-housing scenario. Extra sessions were obtained when a subject exhibited zero target behaviors, if the camera malfunctioned, if a non-subject restricted a subject’s access to the mirror, etc. Test sessions were separated by a minimum of seven days to minimize habituation to the procedure. Subjects were classified as passing (MSR+/+), failing (MSR−/−), or ambiguous (MSR+/−) based on frequency criteria used by Povinelli and colleagues (1993) in chimpanzees. Specifically, subjects that exhibited five or more mirror-guided mark directed responses across the two test sessions were conservatively classified as MSR+/+, between one and four as MSR+/−, and zero as MSR-/−. Using this criterion, 19 were classified as MSR+/+, 18 MSR+/−, and 30 MSR-/−.

Image Collection and Procedure

All chimpanzees were scanned during their annual physical examination. Magnetic resonance image (MRI) scans followed standard procedures at the YNPRC and were designed to minimize stress. Thus, the animals were first sedated with ketamine (10 mg/kg) or telazol (3–5mg/kg) and were subsequently anaesthetized with propofol (40–60 mg/(kg/h)). They were then transported to the MRI scanning facility and placed in a supine position in the scanner with their head in a human-head coil. Upon completion of the MRI, chimpanzees were singly-housed for 2–24 hours to permit close monitoring and safe recovery from the anesthesia prior to returning to their home social group. All procedures were approved by the Institutional Animal Care and Use Committees at YNPRC. The chimpanzees were scanned using a 3.0T G.E. echo-speed Horizon LX MR scanner (Siemens Trio, Siemens Medical Solutions USA, Inc., Malvern, Pennsylvania, USA). T1-weighted images were collected using a three-dimensional gradient echo sequence (pulse repetition= 2300 ms, echo time=4.4 ms, number of signals averaged=3, matrix size =320 X 320).

Cortical Thickness:

The quantification of cortical thickness was performed using FSL (http://fsl.fmrib.ox.ac.uk/fsl/fslwiki/) and FreeSurfer software (https://surfer.nmr.mgh.harvard.edu/) as has been described elsewhere (Hopkins et al., in press). In particular, within FSL each brain was skull striped, bias field corrected and normalised to the standard MNI152 template brain using a 7 degree of freedom transformation (i.e. 3 translations, 3 rotations and 1 uniform scaling). The 7 DoF registration is particularly important to enable the chimpanzee brains to be successfully processed using the FreeSurfer pipeline designed for human brains. The transformation does not alter the morphological shape of the cerebral surface and the uniform scaling factor that is output is recorded as it allows computation of the brain parameters in the real world. Next each brain was segmented using the conventional FreeSurfer process stream. The surface-based module in FreeSurfer enables high quality pial surface reconstruction from the brain volume data by following the signal intensity gradient between grey matter and CSF with subvoxel accuracy (Dale, 1999) on the 3D T1 weighted images. At each surface location (i.e., vertex), the detailed anatomical information (e.g., folding patterns) was also modelled quantitatively by a set of curvature-based descriptors (e.g., the spatial relationship of a vertex to neighbouring vertices). These descriptors later served as natural anatomical landmarks to compute the inter-subject correspondence using a non-linear registration on the sphere space between an individual brain and a reference template through a matching process. As such, the vertex-wise correspondence was determined so as to put all brains in a common coordinate system and this allows convenient vertex-by-vertex comparison in corresponding folds and regions (Fischl, Sereno, Tootell, & Dale, 1999). In this study, the primary focus for the surface-based analysis was cortical thickness (CT). CT at each surface location (or vertex) is defined as the average of the closest distance in either direction between the white and the pial surfaces (Fischl & Dale, 2000). These cortical thickness measures were then merged into a single 4D volume. A Gaussian smoothing with full-width half-maximum of 15 mm was applied to the computed values of cortical thickness to increase the signal-to-noise ratio. A vertex-wise analysis of variance MSR groups were performed using the generalized linear model (GLM) function in FreeSurfer, in which sex was included as nuisance covariates.

Based on an atlas-based labelling technique in FreeSurfer (Desikan et al., 2006), individual brains can be parcellated into 68 gyral based regions (two hemispheres X 34 maps) and average values of CT may be reported for each brain for all these regions. In this case, the chimpanzee brains are warped into human space and the labels are then applied to the homologous regions (Hopkins, Li, Crow, & Roberts, 2017) (see Figure 1). Thus, region specific measures of CT were obtained for the 34 regions within the Desikan-Killiany atlas as applied to the chimpanzee brain. For one analysis, we computed a single mean measure of cortical thickness by averaging the values of the two hemispheres [(R + L)/2]. This allowed us to test for bilateral differences in CT in relation to MSR classification. To test for potential associations between MSR performance and asymmetries in CT, we also computed asymmetry quotients for each region following the formula [AQ=(R-L)/((R+L) *.5)] where R and L represented the thickness values for each hemisphere. We then compared the AQ values for each region between the MSR groups.

Figure 1.

Figure 1

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Illustration of the 34 Desikan maps from the human brain (left panel) warped into the chimpanzee brain (right panel).

Results

Vertex Based Analysis:

Figure 2 shows the regions found to differ between MSR+/+, MSR+/−, and MSR−/− chimpanzees. MSR+/+ apes were found to have increased cortical thickness bilaterally in the caudal ACC and rostral (mostly right hemisphere) ACC and thinner cortex in the central portion of the pre- and postcentral gyri (primarily in the left hemisphere) and left rostral lateral frontal cortex compared to MSR+/− and MSR−/− apes.

Figure 2.

Figure 2

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3D rendering of lateral (upper panel) and medial (lower panel) views of the differences in cortical thickness between MSR+/+, MSR+/− and MSR−/− apes for the vertex-based analysis.

Region-Of-Interest:

For the mean cortical thickness measure, a MANOVA revealed a significant main effect for MSR classification F(68, 56)=1.842, p = .010 and two-way interaction between sex and MSR classification F(68, 56)=1.539, p = .049. For the main effect for MSR classification, subsequent univariate F-tests revealed significant differences for the caudal ACC F(2, 61)=9.307, p = .001, rostral ACC F(2, 61)=3.207, p = .045, posterior cingulate F(2, 61)=4.723, p = .012, precuneus F(2, 61)=3.733, p = .030, and superior parietal F(2, 61)=7.665, p = .001. The mean cortical measures for each region and MSR group are shown in Table 1. For the caudal ACC, post-hoc tests indicated that MSR+/+ chimpanzees had thicker cortex than MSR+/− and MSR−/− apes. Further, MSR+/− apes had thicker cortex than MSR−/− individuals. For the superior frontal cortex, MSR+/+ and MSR+/− apes did not differ in their thickness values but both groups had high values than MSR−/− individuals. For the rostral ACC, posterior cingulate, precuneus and superior parietal, MSR+/− chimpanzees had thicker cortex than MSR−/− apes; however, no significant differences were found between MSR+/+ and MSR−/− apes.

Table 1.

Mean Cortical Thickness for MSR+/+, MSR+/− and MSR−/− Chimpanzees

Brain Region MSR−/− MSR+/+ Brain Region
Bank STS 1.322 (.044) 1.479 (.056) 1.385 (.065)
Caudal Anterior Cingulate 1.439 (.044) 1.707 (.055) 1.685 (.065)
Caudal Middle Frontal 1.648 (.035) 1.719 .044) 1.818 (.051)
Cuneus 1.196 (.028) 1.196 (.036) 1.201 (.042)
Entorhinal 1.926 (.049) 1.868 (.062) 1.882 (.073)
Fusiform 1.343 (.027) 1.342 (.034) 1.302 (.040)
Inferior Parietal 1.318 (028) 1.418 (.035) 1.339 (.041)
Inferior Temporal 1.545 (.030) 1.634 (.038) 1.582 (.044)
Isthmus Cingulate 1.510 (.029) 1.555 (.036) 1.547 (.043)
Lateral Occipital 1.211 (.020) 1.267 (.025) 1.248 (.029)
Lateral Orbital Frontal 2.009 (.033) 2.060 (.042) 1.950 (.049)
Lingual 1.120 (.017) 1.135 (.022) 1.120 (.025)
Medial Orbital Frontal 1.894 (.041) 1.948 (.052) 1.840 (.061)
Middle Temporal 1.627 (.036) 1.738 (.045) 1.628 (.053)
Parahippocampal 1.305 (.040) 1.359 (.051) 1.281 (.060)
Paracentral 1.389 (.039) 1.515 (.050) 1.522 (.058)
Pars Opercularis 1.723 (.032) 1.845 (.041) 1.780 (.048)
Pars Orbitalis 1.946 (.035) 1.928 (.045) 1.951 (.052)
Pars Triangularis 1.739 (.044) 1.804 (.056) 1.722 (.065)
Peri-Calcarine 1.066 (.021) 1.051 (.026) 1.055 (.031)
PostCentral 1.247 (.019) 1.235 (.024) 1.194 (.028)
Posterior Cingulate 1.389 (.039) 1.566 (.050) 1.518 (.058)
PreCentral 1.504 (.036) 1.414 (.046) 1.377 (.054)
Precuneus 1.264 (.027) 1.369 (.034) 1.272 (.040)
Rostral Anterior Cingulate 1.718 (.066) 1.985 (.084) 1.887 (.098)
Rostral Middle Frontal 1.615 (.030) 1.706 (.038) 1.623 (.045)
Superior Frontal 1.919 (.037) 2.047 (.047) 2.051 (.055)
Superior Parietal 1.254 (.020) 1.367 (.025) 1.259 (.029)
Superior Temporal 1.500 (.034) 1.530 (.043) 1.524 (.051)
Supra-Marginal 1.582 (.034) 1.627 (.043) 1.572 (.051)
Frontal Pole 1.811 (.046) 1.811 (.059) 1.876 (.069)
Temporal Pole 2.133 (.057) 2.189 (.073) 2.155 (.085)
Transverse Temporal 1.239 (.041) 1.321 (.052) 1.342 (.061)
Insula 1.826 (.027) 1.882 (.034) 1.838 (.040)
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Values are in mm. Numbers in parentheses are standard errors. Bold values indicate brain regions that revealed significant univariate main effects for MSR classification.

For the two-way interaction between sex and MSR classification, significant univariate effects were found for the caudal ACC F(2, 60)=6.137, p = .004, posterior cingulate F(2, 60)=5.068, p = .009, pars opercularis F(2, 60)=4.875, p = .011, superior frontal F(2, 60)=3.169, p = .049 and superior temporal F(2, 60)=3.996, p = .024 cortex. The mean cortical thickness measures for each of these regions in male and female chimpanzees classified as MSR+/+, MSR+/−, and MSR−/− are shown in Figure 3a to 3e. For all 5 brain regions, MSR+/+ and MSR+/− males had significantly higher values than MSR−/− males while no differences in cortical thickness were found between MSR+/+, MSR+/−, and MSR−/− females. As with the mean cortical measures, we also performed a MANOVA on the AQ scores for each region with sex and MSR group as between group factors. The MANOVA revealed no overall significant main effects or interactions.

Figure 3.

Figure 3

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Mean cortical thickness values (+/− s.e.) for MSR+/+, MSR+/− and MSR−/−male and female chimpanzees. A) Caudal ACC b) Posterior Cingulate c) Pars Opercularis d) Superior Frontal and e) Superior Temporal

Discussion

The results of this study are fairly straightforward. Measuring cortical thickness using a vertex- and ROI approach, we found that MSR+/+ chimpanzees had higher values than MSR−/− apes in several brain regions including the caudal, rostral and posterior cingulate cortex as well as the inferior frontal and superior frontal gyrus, particularly among males. When comparing the findings from the two analytic approaches, the regions consistently implicated in MSR performance were largely similar within the rostral and caudal anterior cingulate and superior frontal cortex.

The evidence that cortical thickness, particularly within the anterior portions of the cingulate cortex is associated with MSR is of specific theoretical interest. Although not directly assessed in the current study, studies have reported the abundance of spindle cells or Von Economo neurons (VENs) in the cerebral cortex of human and nonhuman animals, including great apes (Nimchinsky et al., 1999), whales, dolphins (Hof, Chanis, & Marino, 2005; Hof & Van der Gucht, 2007) and elephants (Hakeem et al., 2009) but these neurons are absent or only sparsely concentrated in more distantly related primates and other mammalian species (Allman et al., 2010; Evrard, Forro, & Logothetis, 2012; Nimchinsky et al., 1999). Among human and nonhuman primates, VENs are richly concentrated in layer V of the ACC and frontal insular (FI) cortex but have also been found in dorsolateral prefrontal cortex (Allman et al., 2010; Fajardo et al., 2008; Nimchinsky et al., 1999; von Economo & Koskinas, 1925). Importantly, some have hypothesized that the presence of VENs in human and great apes and the scarcity or absence of VENs in more distantly related primates may be related to the evolution of more complex social cognition, including MSR (Allman, Tetreault, Hakeem, & Park, 2011). This link is further supported by studies in clinical populations showing that atypical development or loss of VENs may be associated with neurodegenerative disorders such as fronto-temporal dementia (Levensen & Miller, 2007; Seeley et al., 2006) and neurodevelopmental disorders including autism and early onset schizophrenia (Brune et al., 2010; Santos et al., 2011). Each of these disorders is characterized, in part, by dysfunction in social cognition including a loss or limitation in self-awareness abilities. Though our findings do not directly implicate VENs in MSR performance, they are consistent with the view that the ACC and the neurons residing within this region play a role in MSR abilities and may be involved in cognitive and emotional processes that are predicated on the existence of self-recognition or an interoceptive awareness of one’s own body states (Nieuwenhuys, 2012).

Differences between MSR groups were also found for the inferior frontal gyrus (IFG), particularly in males. The IFG in chimpanzees is the homolog to the Pars opercularis and Brodmann’s area 44 (BA44) in the human brain and therefore constitutes part of Broca’s area. Indeed, cytoarchitectonic analysis of chimpanzee post-mortem brains have shown that BA44 cells are more consistently found in the IFG of the chimpanzee brain (Schenker et al., 2010). Further, as is the case in human brains, morphologically the IFG is bordered anteriorly by the fronto-orbital sulcus, superiorly by the inferior frontal sulcus and posteriorly by the PCI in the chimpanzee brain (Keller, Crow, Foundas, Amunts, & Roberts, 2009; Keller, Deppe, Herbin, & Gilissen, 2012; Keller, Roberts, & Hopkins, 2009). Importantly, in a recent study examining white matter connectivity in relation to MSR performance in chimpanzees, Hecht et al. (2017) reported that MSR+/+ chimpanzees differed from MSR+/− and MSR−/− chimpanzees in the number of terminations of the SLF in GM within the right IFG. The ROI cortical thickness results reported here are consistent with the DTI results in implicating the IFG in MSR performance, particularly within the superior region of this gyrus. It should be noted that the same chimpanzees were subjects in both this and the Hecht et al study.

One limitation of this study was the criteria used to classify performance on the self-recognition task. As others have done (Povinelli et al., 1993), we used rather conservative criteria for classifying apes as passing or failing our version of the mark test. Indeed, more chimpanzees passed than failed our version of the mark test when excluding those individuals that produced fewer than 5 mouth mark–directed responses. When including those producing between 1 and 5 mouth mark-directed responses within the MSR+/+ sample, a slight majority of chimpanzees passed the test. Interestingly, though there were some cortical thickness differences found between MSR+/+ and MSR+/− and the bulk of the differences were evident between the MSR+/+ and MSR+/− apes compared to the MSR- apes, notably in males. Thus, from the standpoint of neurological differences, there does not appear to be a robust distinction between MSR+/+ and MSR+/− apes but significant differences between these two cohorts and MSR −/− chimpanzees. As we have indicated in previous studies using these methods (Hopkins et al., 2017), an additional limitation is our use of the human Desikan maps to identify regions of interest in the chimpanzee brain. Though we believe the homology in the regions of interest are pretty good, there are cellular and morphological differences in the human and chimpanzee brain that do not align. Thus, further development of a chimpanzee specific set of region-of-interest maps would be very useful.

Limitations notwithstanding, results of the current study contribute to our understanding of brain systems that may give rise to individual differences in MSR abilities. Underscoring the importance of this ability is the recently developed National Institute of Mental Health’s (NIMH) Research Domain Criteria (RDOC; Insel et al., 2010; Kozak & Cuthbert, 2016), which aims to elucidate the neurobiological bases of mental illness and reframe conceptions of psychopathology around constructs with specific brain referents. The RDoC research framework specifies constructs, grouped within major domains of functioning, as explanatory referents for understanding clinical problems. Within the RDoC Social Processes domain, the construct of “Perception and Understanding of Self” is included as one important focus for research. Individual variability in MSR abilities appear to fit clearly within this domain; thus investigations of the foundation of variation in these abilities among chimpanzees, an animal species uniquely well-suited for research on broad, transdiagnostic traits (Latzman & Hopkins, 2016; Latzman, Young, & Hopkins, 2016) provide an important contribution to the larger RDoC effort.

Further, to the extent these brains systems co-vary with other measures of social cognition or are restricted to MSR warrants further investigation but it seems reasonable to assume that other cognitive processes may underlie the observed associations reported here. It is difficult to argue that there was direct selection for increasing and explicit MSR abilities, among primates, in light of the fact that there are few instances in the natural world where exposure to reflective surfaces would be both available and have some functional or adaptive significance. Thus, it seems likely the neural systems underlying MSR, as reported here, likely reflect other, as yet to be determined, social cognitive processes that were under increased selection pressure. Further investigations on the covariation in function between MSR and other cognitive processes will provide important insight into the neural systems involving social cognition and intelligence from an evolutionary perspective.

Acknowledgement

This research was supported in part by NIH grants NS-73134, NS-42867, and HD-60563. American Psychological Association guidelines for the ethical treatment of animals were adhered to during all aspects of this study. We are grateful to the helpful assistance of the entire veterinary staff at the YNPRC for their assistance in collection of the MRI scans.

Footnotes

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