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A neuroanatomical predictor of mirror self-recognition in chimpanzees.

ABSTRACT: The ability to recognize one's own reflection is shared by humans and only a few other species, including chimpanzees. However, this ability is highly variable across individual chimpanzees. In humans, self-recognition involves a distributed, right-lateralized network including frontal and parietal regions involved in the production and perception of action. The superior longitudinal fasciculus (SLF) is a system of white matter tracts linking these frontal and parietal regions. The current study measured mirror self-recognition (MSR) and SLF anatomy in 60 chimpanzees using diffusion tensor imaging. Successful self-recognition was associated with greater rightward asymmetry in the white matter of SLFII and SLFIII, and in SLFIII's gray matter terminations in Broca's area. We observed a visible progression of SLFIII's prefrontal extension in apes that show negative, ambiguous, and compelling evidence of MSR. Notably, SLFIII's terminations in Broca's area are not right-lateralized or particularly pronounced at the population level in chimpanzees, as they are in humans. Thus, chimpanzees with more human-like behavior show more human-like SLFIII connectivity. These results suggest that self-recognition may have co-emerged with adaptations to frontoparietal circuitry.

SUBMITTER: Hecht EE

PROVIDER: S-EPMC5390703 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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A neuroanatomical predictor of mirror self-recognition in chimpanzees.

Hecht E E EE Mahovetz L M LM Preuss T M TM Hopkins W D WD

Social cognitive and affective neuroscience 20170101 1

The ability to recognize one's own reflection is shared by humans and only a few other species, including chimpanzees. However, this ability is highly variable across individual chimpanzees. In humans, self-recognition involves a distributed, right-lateralized network including frontal and parietal regions involved in the production and perception of action. The superior longitudinal fasciculus (SLF) is a system of white matter tracts linking these frontal and parietal regions. The current study ...[more]

PMID: 27803287

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Project description:SEE SARAZIN ET AL DOI101093/BRAIN/AWW041 FOR A SCIENTIFIC COMMENTARY ON THIS ARTICLE: The advent of the positron emission tomography tracer (18)F-AV1451 provides the unique opportunity to visualize the regional distribution of tau pathology in the living human brain. In this study, we tested the hypothesis that tau pathology is closely linked to symptomatology and patterns of glucose hypometabolism in Alzheimer's disease, in contrast to the more diffuse distribution of amyloid-β pathology. We included 20 patients meeting criteria for probable Alzheimer's disease dementia or mild cognitive impairment due to Alzheimer's disease, presenting with a variety of clinical phenotypes, and 15 amyloid-β-negative cognitively normal individuals, who underwent (18)F-AV1451 (tau), (11)C-PiB (amyloid-β) and (18)F-FDG (glucose metabolism) positron emission tomography, apolipoprotein E (APOE) genotyping and neuropsychological testing. Voxel-wise contrasts against controls (at P < 0.05 family-wise error corrected) showed that (18)F-AV1451 and (18)F-FDG patterns in patients with posterior cortical atrophy ('visual variant of Alzheimer's disease', n = 7) specifically targeted the clinically affected posterior brain regions, while (11)C-PiB bound diffusely throughout the neocortex. Patients with an amnestic-predominant presentation (n = 5) showed highest (18)F-AV1451 retention in medial temporal and lateral temporoparietal regions. Patients with logopenic variant primary progressive aphasia ('language variant of Alzheimer's disease', n = 5) demonstrated asymmetric left greater than right hemisphere (18)F-AV1451 uptake in three of five patients. Across 30 FreeSurfer-defined regions of interest in 16 Alzheimer's disease patients with all three positron emission tomography scans available, there was a strong negative association between (18)F-AV1451 and (18)F-FDG uptake (Pearson's r = -0.49 ± 0.07, P < 0.001) and less pronounced positive associations between (11)C-PiB and (18)F-FDG (Pearson's r = 0.16 ± 0.09, P < 0.001) and (18)F-AV1451 and (11)C-PiB (Pearson's r = 0.18 ± 0.09, P < 0.001). Voxel-wise linear regressions thresholded at P < 0.05 (uncorrected) showed that, across all patients, younger age was associated with greater (18)F-AV1451 uptake in wide regions of the neocortex, while older age was associated with increased (18)F-AV1451 in the medial temporal lobe. APOE ϵ4 carriers showed greater temporal and parietal (18)F-AV1451 uptake than non-carriers. Finally, worse performance on domain-specific neuropsychological tests was associated with greater (18)F-AV1451 uptake in key regions implicated in memory (medial temporal lobes), visuospatial function (occipital, right temporoparietal cortex) and language (left > right temporoparietal cortex). In conclusion, tau imaging-contrary to amyloid-β imaging-shows a strong regional association with clinical and anatomical heterogeneity in Alzheimer's disease. Although preliminary, these results are consistent with and expand upon findings from post-mortem, animal and cerebrospinal fluid studies, and suggest that the pathological aggregation of tau is closely linked to patterns of neurodegeneration and clinical manifestations of Alzheimer's disease.

Dataset Information

A neuroanatomical predictor of mirror self-recognition in chimpanzees.

Publications

A neuroanatomical predictor of mirror self-recognition in chimpanzees.

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