Erin Hecht

Process Versus Product in Social Learning: Comparative Diffusion Tensor Imaging of Neural Systems for Action Execution–Observation Matching in Macaques, Chimpanzees, and Humans

Social learning varies among primate species. Macaques only copy the product of observed actions, or emulate, while humans and chimpanzees also copy the process, or imitate. In humans, imitation is linked to the mirror system. Here we compare mirror system connectivity across these species using diffusion tensor imaging. In macaques and chimpanzees, the preponderance of this circuitry consists of frontal-temporal connections via the extreme/external capsules. In contrast, humans have more substantial temporal-parietal and frontal-parietal connections via the middle/inferior longitudinal fasciculi and the third branch of the superior longitudinal fasciculus. In chimpanzees and humans, but not in macaques, this circuitry includes connections with inferior temporal cortex. In humans alone, connections with superior parietal cortex were also detected. We suggest a model linking species differences in mirror system connectivity and responsivity with species differences in behavior, including adaptations for imitation and social learning of tool use.

Virtual dissection and comparative connectivity of the superior longitudinal fasciculus in chimpanzees and humans.

Many of the behavioral capacities that distinguish humans from other primates rely on fronto-parietal circuits. The superior longitudinal fasciculus (SLF) is the primary white matter tract connecting lateral frontal with lateral parietal regions; it is distinct from the arcuate fasciculus, which interconnects the frontal and temporal lobes. Here we report a direct, quantitative comparison of SLF connectivity using virtual in vivo dissection of the SLF in chimpanzees and humans. SLF I, the superior-most branch of the SLF, showed similar patterns of connectivity between humans and chimpanzees, and was proportionally volumetrically larger in chimpanzees. SLF II, the middle branch, and SLF III, the inferior-most branch, showed species differences in frontal connectivity. In humans, SLF II showed greater connectivity with dorsolateral prefrontal cortex, whereas in chimps SLF II showed greater connectivity with the inferior frontal gyrus. SLF III was right-lateralized and proportionally volumetrically larger in humans, and human SLF III showed relatively reduced connectivity with dorsal premotor cortex and greater extension into the anterior inferior frontal gyrus, especially in the right hemisphere. These results have implications for the evolution of fronto-parietal functions including spatial attention to observed actions, social learning, and tool use, and are in line with previous research suggesting a unique role for the right anterior inferior frontal gyrus in the evolution of human fronto-parietal network architecture.

Evolutionary neuroscience of cumulative culture

Culture suffuses all aspects of human life. It shapes our minds and bodies and has provided a cumulative inheritance of knowledge, skills, institutions, and artifacts that allows us to truly stand on the shoulders of giants. No other species approaches the extent, diversity, and complexity of human culture, but we remain unsure how this came to be. The very uniqueness of human culture is both a puzzle and a problem. It is puzzling as to why more species have not adopted this manifestly beneficial strategy and problematic because the comparative methods of evolutionary biology are ill suited to explain unique events. Here, we develop a more particularistic and mechanistic evolutionary neuroscience approach to cumulative culture, taking into account experimental, developmental, comparative, and archaeological evidence. This approach reconciles currently competing accounts of the origins of human culture and develops the concept of a uniquely human technological niche rooted in a shared primate heritage of visuomotor coordination and dexterous manipulation.

Early life stress affects cerebral glucose metabolism in adult rhesus monkeys (Macaca mulatta).

Early life stress (ELS) is a risk factor for anxiety, mood disorders and alterations in stress responses. Less is known about the long-term neurobiological impact of ELS. We used [(18)F]-fluorodeoxyglucose Positron Emission Tomography (FDG-PET) to assess neural responses to a moderate stress test in adult monkeys that experienced ELS as infants. Both groups of monkeys showed hypothalamic-pituitary-adrenal (HPA) axis stress-induced activations and cardiac arousal in response to the stressor. A whole brain analysis detected significantly greater regional cerebral glucose metabolism (rCGM) in superior temporal sulcus, putamen, thalamus, and inferotemporal cortex of ELS animals compared to controls. Region of interest (ROI) analyses performed in areas identified as vulnerable to ELS showed greater activity in the orbitofrontal cortex of ELS compared to control monkeys, but greater hippocampal activity in the control compared to ELS monkeys. Together, these results suggest hyperactivity in emotional and sensory processing regions of adult monkeys with ELS, and greater activity in stress-regulatory areas in the controls. Despite these neural responses, no group differences were detected in neuroendocrine, autonomic or behavioral responses, except for a trend towards increased stillness in the ELS monkeys. Together, these data suggest hypervigilance in the ELS monkeys in the absence of immediate danger.

What can other animals tell us about human social cognition? An evolutionary perspective on reflective and reflexive processing

Human neuroscience has seen a recent boom in studies on reflective, controlled, explicit social cognitive functions like imitation, perspective-taking, and empathy. The relationship of these higher-level functions to lower-level, reflexive, automatic, implicit functions is an area of current research. As the field continues to address this relationship, we suggest that an evolutionary, comparative approach will be useful, even essential. There is a large body of research on reflexive, automatic, implicit processes in animals. A growing perspective sees social cognitive processes as phylogenically continuous, making findings in other species relevant for understanding our own. One of these phylogenically continuous processes appears to be self-other matching or simulation. Mice are more sensitive to pain after watching other mice experience pain; geese experience heart rate increases when seeing their mate in conflict; and infant macaques, chimpanzees, and humans automatically mimic adult facial expressions. In this article, we review findings in different species that illustrate how such reflexive processes are related to (“higher order”) reflexive processes, such as cognitive empathy, theory of mind, and learning by imitation. We do so in the context of self-other matching in three different domains—in the motor domain (somatomotor movements), in the perceptual domain (eye movements and cognition about visual perception), and in the autonomic/emotional domain. We also review research on the developmental origin of these processes and their neural bases across species. We highlight gaps in existing knowledge and point out some questions for future research. We conclude that our understanding of the psychological and neural mechanisms of self-other mapping and other functions in our own species can be informed by considering the layered complexity these functions in other species.

Brain organization of gorillas reflects species differences in ecology

Gorillas include separate eastern (Gorilla beringei) and western (Gorilla gorilla) African species that diverged from each other approximately 2 million years ago. Although anatomical, genetic, behavioral, and socioecological differences have been noted among gorilla populations, little is known about variation in their brain structure. This study examines neuroanatomical variation between gorilla species using structural neuroimaging. Postmortem magnetic resonance images were obtained of brains from 18 captive western lowland gorillas (Gorilla gorilla gorilla), 15 wild mountain gorillas (Gorilla beringei beringei), and 3 Grauers gorillas (Gorilla beringei graueri) (both wild and captive). Stereologic methods were used to measure volumes of brain structures, including left and right frontal lobe gray and white matter, temporal lobe gray and white matter, parietal and occipital lobes gray and white matter, insular gray matter, hippocampus, striatum, thalamus, each hemisphere and the vermis of the cerebellum, and the external and extreme capsules together with the claustrum. Among the species differences, the volumes of the hippocampus and cerebellum were significantly larger in G. gorilla than G. beringei. These anatomical differences may relate to divergent ecological adaptations of the two species. Specifically, G. gorilla engages in more arboreal locomotion and thus may rely more on cerebellar circuits. In addition, they tend to eat more fruit and have larger home ranges and consequently might depend more on spatial mapping functions of the hippocampus.

Intranasal oxytocin reduces social perception in women: Neural activation and individual variation

ABSTRACT Most intranasal oxytocin research to date has been carried out in men, but recent studies indicate that females’ responses can differ substantially from males’. This randomized, double‐blind, placebo‐controlled study involved an all‐female sample of 28 women not using hormonal contraception. Participants viewed animations of geometric shapes depicting either random movement or social interactions such as playing, chasing, or fighting. Probe questions asked whether any shapes were “friends” or “not friends.” Social videos were preceded by cues to attend to either social relationships or physical size changes. All subjects received intranasal placebo spray at scan 1. While the experimenter was not blinded to nasal spray contents at Scan 1, the participants were. Scan 2 followed a randomized, double‐blind design. At scan 2, half received a second placebo dose while the other half received 24 IU of intranasal oxytocin. We measured neural responses to these animations at baseline, as well as the change in neural activity induced by oxytocin. Oxytocin reduced activation in early visual cortex and dorsal‐stream motion processing regions for the social > size contrast, indicating reduced activity related to social attention. Oxytocin also reduced endorsements that shapes were “friends” or “not friends,” and this significantly correlated with reduction in neural activation. Furthermore, participants who perceived fewer social relationships at baseline were more likely to show oxytocin‐induced increases in a broad network of regions involved in social perception and social cognition, suggesting that lower social processing at baseline may predict more positive neural responses to oxytocin. HIGHLIGHTSA randomized, double‐blind, placebo‐controlled fMRI study of intranasal oxytocin.Neural response of females was measured during animations of interacting shapes.Oxytocin (OXT) reduced activation in early visual cortex and dorsal stream regions.OXT reduced perception of social relationships.OXT increased social cognition networks in females with lower baseline perception

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.

Techniques for Studying Brain Structure and Function

Recent years have seen rapid improvement in neuroscience techniques for studying brain structure and function in humans and our primate relatives. These techniques offer new routes of inquiry into our evolutionary history. This chapter offers an overview of a collection of these methods, including discussion of each techniques strengths, weaknesses, and relevance to neuroarchaeology.

Adaptations to vision-for-action in primate brain evolution: Comment on "Towards a Computational Comparative Neuroprimatology: Framing the language-ready brain" by Michael A. Arbib.

As Arbib [1] notes, the two-streams hypothesis [5] has provided a powerful explanatory framework for understanding visual processing. The inferotemporal ventral stream recognizes objects and agents – “what” one is seeing. The dorsal “how” or “where” stream through parietal cortex processes motion, spatial location, and visuo-proprioceptive relationships – “vision for action.” Hickock and Poeppel’s [3] extension of this model to the auditory system raises the question of deeper, multior supra-sensory themes in dorsal vs. ventral processing. Petrides and Pandya [10] postulate that the evolution of language may have been influenced by the fact that the dorsal stream terminates in posterior Broca’s area (BA44) while the ventral stream terminates in anterior Broca’s area (BA45). In an intriguing potential parallel, a recent ALE metanalysis of 54 fMRI studies found that semantic processing is located more anteriorly and superiorly than syntactic processing in Broca’s area [13]. But clearly, macaques do not have language, nor other likely preor co-adaptations to language, such as complex imitation and tool use. What changed in the brain that enabled these functions to evolve? Early conceptualizations of the two-streams hypothesis focused on similarities between monkey and human brain organization. At the time, there simply was not a way to study considerable numbers of healthy, living nonhuman primate and human brains in a directly comparative manner. More recently, though, advancements in neuroimaging have made this possible, and now mounting evidence points toward both functional and structural elaboration of the human dorsal stream. Relative to macaques, humans show unique responsivity to 3D-form-from-motion stimuli in the intraparietal sulcus [16], unique responsivity for observed tool use in the anterior supramarginal gyrus [11], and reduced prefrontal activation during the observation of objects [2]. Relative to chimpanzees, humans show similar co-activation between executed action and both transitive and intransitive observed action, in homologues to macaque mirror regions, but a differential distribution of activation during grasping observation, with chimp activation being largely prefrontallyfocused and human activation showing increases in occipitotemporal and parietal cortex [7]. Interestingly, the finding