Erin E. Hecht - US grants

DESCRIPTION (provided by applicant): The proposed research will compare behavior, functional brain responses, and anatomical connectivity in the mirror system in macaques, chimpanzees, and humans. The mirror system is thought to underlie action understanding by allowing individuals to simulate others'actions as if they were performing them. However, several unresolved issues limit the extent to which the mirror system can be linked to human social cognition. First, macaque mirror system results are largely replicated. Second, the equivalence between macaque and human results is unclear because they involve different methodologies. Third, macaque and human mirror system responses differ, with only the human mirror system responding to actions that do not involve objects. Fourth, macaques lack some behaviors which have been linked to the mirror system in humans, most notably imitation. This proposal will address the first two issues by validating basic macaque mirror system findings using a methodology comparable to those used in humans. It will address the second two issues by directly investigating how mirror system responses and connectivity differ among primate species. The main hypothesis is that an evolved broadening in mirror system response properties, via increased connectivity with other brain networks, allowed these cells to respond to, and thus simulate, a wider variety of observed stimuli. This hypothesis will be tested using a combination of behavioral tasks, in vivo functional neuroimaging, and structural diffusion tensor imaging. Aim 1 will employ 18F-FDG positron emission tomography to compare the neural correlates of the execution and observation of actions with and without objects in macaques and chimpanzees. Aim 1 will also procure behavioral indices of imitation ability in each subject. Aim 2 will use diffusion tensor imaging to compare white matter pathways linking the components of the mirror system in macaques, chimpanzees, and humans. The behavioral and functional brain responses obtained in Aim 1 will be compared to the anatomical results obtained in Aim 2. In this way, species and individual differences in imitation ability can be linked to differences in brain responses and anatomical connectivity. PUBLIC HEALTH RELEVANCE: Disorders like autism and schizophrenia affect social skills like the ability to link perceived facial expressions to internal emotional states and the ability to infer goals and intentions from observed actions. These disorders appear to be uniquely human, and the abilities they affect are developed in humans to an extent not seen in other primates. Because these abilities reflect a recent evolutionary change in function, identification of the underlying evolutionary changes in anatomy can locate potential foci for these diseases.

This project will investigate features of neural system organization that can be linked to altered social behavior, including reduced or increased aggression. Two species of canids, experimentally domesticated silver foxes (Vulpes vulpes) and domestic dogs (Canis familiaris), have been selectively bred by humans for altered social behavior. These behavioral changes occurred alongside a restricted set of genetic changes, creating an unparalleled opportunity to link the evolution of behavioral characteristics (phenotypes) to neural phenotypes. Recent technological advancements enable detailed, non-invasive studies of brain anatomy at relatively low cost. This project will take advantage of these innovations to create high-resolution three-dimensional (3D) brain maps using structural magnetic resonance imaging, diffusion tensor imaging, and digitized histology. Expected products of this research include: (1) identification of features of neural organization that are linked to reduced or increased sociality or aggression, expected to be generalizable to other species, (2) the production of online fox and dog brain atlases that will be publicly available as a research tool for the general scientific community, (3) training opportunities for young scientists, and (4) outreach efforts using blog and social media posts for the general public. Because dogs are a "common denominator" across various cultures, this research has a unique opportunity to be personally relevant and compelling to people from all walks of society, and to enhance public appreciation for science.

Both experimentally-domesticated foxes and domestic dogs are distinguished from their wild forebears by altered social approach-avoidance behavior. Previous research in rodents and primates, and the researchers' own preliminary data, allow for the formation of well-grounded hypotheses about neural adaptations that result from selection pressure on social approach-avoidance behavior. Specifically, this project will investigate limbic and fronto-limbic systems governing social behavior and response selection. In order to identify features of neural system organization associated with altered social behavior, whole-brain white and gray matter organization will be compared (a) between various breeds of domestic dogs, each tested for social approach-avoidance/aggression behavior, and (b) between strains of foxes bred for social avoidance behavior, which react aggressively to social contact, versus foxes bred for social approach behavior, which are tame and friendly like dogs, versus wild type foxes. Whole-brain MRI and DTI images will be collected using 3.0 and 9.4 Tesla MRI scanners. Histology images will be digitally scanned and aligned to MRI images. Analyses will include voxel-based morphometry, tract-based spatial statistics, probabilistic tractography, and k-means connectivity-based parcellation. The research will advance knowledge about how evolution modified brain organization in response to selection for social approach and avoidance.

Humans have remarkably plastic brains; adaptations for learning are perhaps the hallmark evolutionary trait of our species. This project will examine learning-related aspects of brain organization in great ape species that are close evolutionary relatives of humans – bonobos and chimpanzees – using noninvasive tests and archived brain samples and images. The work focuses on two learned skills that were important factors in human evolution: tool use and language. One analysis will use archived brain images from previous studies combined with new behavioral tests of skill learning. Apes will receive training in evolutionarily-relevant, naturalistic tool use skills, and the investigators will measure how individual variation in brain organization is related to skill learning. Another analysis will examine brain organization in apes that have and have not undergone training to use language-like systems, including hand signs and pictogram boards. The investigators will examine how language training is related to learning-related changes in the brain. Results are expected to shed light on probable brain changes during the evolution of the human species, provide insight on neural mechanisms of real-world skill learning in primate species closely related to humans, and facilitate understanding of how individual variation in brain structure is related to individual variation in behavior and cognition.<br/> <br/>This project will use a cross-disciplinary, comparative, integrative approach to examine how individual variation in brain anatomy influences learning trajectories in the context of real-world, evolutionarily relevant skills. It also examines the interaction between acquired, plastic changes in the brain resulting from learning during an individual’s lifetime, and evolved, heritable changes resulting from natural selection across generations. The project brings together methodological and theoretical approaches from neuroscience and neuroimaging, anthropology, archaeology, and animal behavior. Identification of plastic changes resulting from language training in great apes will provide a new window on the evolution of language circuits in our own species and will for the first time add crucial neurobiological information to landmark, long-running language-training studies in apes. Additionally, individual variation in chimpanzee and bonobo brain anatomy will be linked to differences in learning trajectories in two evolutionarily-relevant, real-world skills: simple stone tool knapping and nut cracking. Together, this research will provide important new insight on brain changes underlying acquisition of learned skills both on the timescale of individual lifetimes (plasticity) and the timescale of evolved, species-level change (adaptation).<br/><br/>This project is funded by the Integrated Strategies for Understanding Neural and Cognitive Systems (NCS) program, which is jointly supported by the Directorates for Computer and Information Science and Engineering (CISE), Education and Human Resources (EHR), Engineering (ENG), and Social, Behavioral, and Economic Sciences (SBE).<br/><br/>This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.