Periodic Reporting for period 1 - HumanUniqueness (Does the temporal cortex make humans special? What comparing the human and great ape brain can tell us about cognitive evolution) Reporting period: 2017-09-01 to 2019-08-31 Summary of the context and overall objectives of the project What is the problem/issue being addressed?Humans are unique in their ability to process complex conceptual information. To understand how humans evolved this ability, we need to know what neuroanatomical specializations support this behavior. Evidence has pointed to several candidate areas within the temporal lobe that are important for human conceptual processing. These areas also appear to have expanded disproportionately since our divergence from Old World monkeys. This project sought to both identify the functional correlates of conceptual processing in humans and to characterize the structural organization of these territories in humans, chimpanzees, and macaques, in order to determine what structural components are evolutionarily novel and which are shared with our primate relatives.Why is it important for society?The similarities between humans and primates, especially chimpanzees, have been emphasized to the public for many years. However, we still struggle to precisely delineate the differences in cognitive abilities between ourselves and other primates. Understanding the structural basis of conceptual processing in humans has important health implications as well, as it is affected by a variant of fronto-temporal dementia known semantic dementia, also known as semantic variant primary progressive aphasia. What are the overall objectives?The overall objective was to advance our understanding of how the human brain became capable of processing conceptual information, which we hypothesized is related to anatomical specializations in the human temporal cortex. To identify the cortical areas involved, two fMRI studies were designed. To identify to what extent these areas are similar to our primate relatives, diffusion scans of the brains of humans, great apes, and monkeys were analyzed to build comparative white matter atlases and surface-based connectivity parcellations. What are the conclusions of the action?The research from this action identified (1) cortical regions in humans that are organizationally different from chimpanzees and macaques, (2) which modifications occurred prior and after our split with the great apes. (3) key white matter tracts that are driving these differences and (4) neural correlates of category versus conceptual processing in humans. Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far A tractography atlas was created with 29 chimpanzee scans with comparable atlases for humans and rhesus macaques (fig. 1). These data were used to compute cortical surface projections, cortical fingerprints, and cortical blueprints. Two fMRI projects were designed to probe object categorization and to disambiguate the processing of concepts, narrative, and social stimuli. ResultsAtlas results (1) replicated known differences between humans, chimpanzees, and macaques regarding the arcuate fasciculus, (2) identified modifications to the superior longitudinal fasciculus system unique to humans, and (3) found modifications to the inferior fronto-occipital fasciculus unique to humans, which has implications for human ventral stream visual processing, which has a role in conceptual processing.Cortical blueprint results (fig. 2) indicate changes to white matter in human and hominoid lineages in the temporal lobes, as we had hypothesized, but also in inferior parietal areas. Differences between humans and macaques also included changes to lateral prefrontal areas. Thus humans and great apes appear to share modifications to prefrontal white matter, while parietal and posterior temporal white matter was modified after humans diverged from other great apes. Our fMRI category and conceptual processing project found prefrontal areas, in concert with early visual areas, are involved in processes that support differentiating concepts into categories. This supports an enactivist model of conceptual processing. The results from this study, combined with preliminary findings from a colleague, lead us to design the second fMRI study, in which participants are exposed to longer duration stimuli in an effort to better understand the relationship between conceptual processing and social and other contextual cues. DisseminationFour conference posters were presented - (Cortical Evolution Conference, Spain, Society for Neuroscience Conference, USA, Organization for Human Brain Mapping Conference, Italy). Four talks were given (J.B. Johnston Club, USA, Max Planck Institute for Psycholinguistics, NL, Comparative MRI, DE, Bias in AI and Neuroscience Conference, NL). I co-authored 4 additional poster presentations and a conference talk. A paper on white matter mapping (2018), and on the intersection of feminist science and neuroimaging (2019) were published. A book chapter on the human temporal lobe was published (2018) and another is in final editing. Three papers are in preparation, based on the chimpanzee atlas, the blueprint data, and the first fMRI study; a fourth paper is anticipated from the second fMRI project.I co-organized two international conferences during the grant period - one on the role of bias in AI and neuroscience, held at the host institution (2019) and one on the interface of gender studies and neuroscience, to be held in the host country in 2020. I was also interviewed for a Dutch documentary and for a column in the Dutch newspaper of record. Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far) The project implemented a novel cortical blueprint methodology which permitted direct comparison of white matter projections to cortex across species. By using this method with three related species, we were able to perform a phylogenetic analysis. Going forward, this method can be applied to a wide variety of species in order to retrace the evolutionary trajectory of the human brain, a burgeoning field within evolutionary neuroscience which could be termed "neurophylogenetics" (figure 3). The second fMRI study involves a novel paradigm in which medium length video stimuli are used to identify long duration temporal activation. The study involves hyperalignment and inter-subject correlation, which have not been used to probe the functioning of this area of the brain before.Data collection for the second fMRI project will end by December 2019, with data analysis beginning in January 2020. The chimpanzee atlas and cortical blueprint maps will be mined for future quantitative comparisons of human, chimpanzee, and macaque white matter organization. This will involve examinations of tract volume, proportion, lateralization, and inter-individual variability.Potential impacts of these results include contributing to the standardization of protocols for delineating white matter tracts across species. This streamlining of atlasing will permit the rapid acquisition of knowledge on brain evolution. These results will also shed light on the role of conceptual processing in social cognition, and how this may relate to the comprehension of narrative. This can help illuminate the phenomenology of conceptual processing, which is a hotly debated topic for neuroscientists and philosophers. Figure 2: A portion of the cortical blueprint results (humans vs. chimps) Figure 1: A portion of the white matter atlas for chimpanzees Figure 3: A neurophylogenetic tree from the cortical blueprint results
