In humans, the wakeful resting condition is characterized by a default mode of brain function involving high levels of activity within a functionally connected network of brain regions. This network has recently been implicated in mental self-projection into the past, the future, or another individual's perspective. Here we use [18F]-fluorodeoxyglucose positron emission tomography imaging to assess resting-state brain activity in our closest living relative, the chimpanzee, as a potential window onto their mental world and compare these results with those of a human sample. We find that, like humans, chimpanzees show high levels of activity within default mode areas, including medial prefrontal and medial parietal cortex. Chimpanzees differ from our human sample in showing higher levels of activity in ventromedial prefrontal cortex and lower levels of activity in left-sided cortical areas involved in language and conceptual processing in humans. Our results raise the possibility that the resting state of chimpanzees involves emotionally laden episodic memory retrieval and some level of mental self-projection, albeit in the absence of language and conceptual processing.
The precuneus is a major element of the superior parietal lobule, positioned on the medial side of the hemisphere and reaching the dorsal surface of the brain. It is a crucial functional region for visuospatial integration, visual imagery, and body coordination. Previously, we argued that the precuneus expanded in recent human evolution, based on a combination of paleontological, comparative, and intraspecific evidence from fossil and modern human endocasts as well as from human and chimpanzee brains. The longitudinal proportions of this region are a major source of anatomical variation among adult humans and, being much larger in Homo sapiens, is the main characteristic differentiating human midsagittal brain morphology from that of our closest living primate relative, the chimpanzee. In the current shape analysis, we examine precuneus variation in non-human primates through landmark-based models, to evaluate the general pattern of variability in non-human primates, and to test whether precuneus proportions are influenced by allometric effects of brain size. Results show that precuneus proportions do not covary with brain size, and that the main difference between monkeys and apes involves a vertical expansion of the frontal and occipital regions in apes. Such differences might reflect differences in brain proportions or differences in cranial architecture. In this sample, precuneus variation is apparently not influenced by phylogenetic or allometric factors, but does vary consistently within species, at least in chimpanzees and macaques. This result further supports the hypothesis that precuneus expansion in modern humans is not merely a consequence of increasing brain size or of allometric scaling, but rather represents a species-specific morphological change in our lineage.
Interregional connections of the brain measured with diffusion tractography can be used to infer valuable information regarding both brain structure and function. However, different tractography algorithms can generate networks that exhibit different characteristics, resulting in poor reproducibility across studies. Therefore, it is important to benchmark different tractography algorithms to quantitatively assess their performance. Here we systematically evaluated a newly introduced tracking algorithm, global tractography, to derive anatomical brain networks in a fiber phantom, 2 post-mortem macaque brains, and 20 living humans, and compared the results with an established local tracking algorithm. Our results demonstrated that global tractography accurately characterized the phantom network in terms of graph-theoretic measures, and significantly outperformed the local tracking approach. Results in brain tissues (post-mortem macaques and in vivo humans), however, showed that although the performance of global tractography demonstrated a trend of improvement, the results were not vastly different than that of local tractography, possibly resulting from the increased fiber complexity of real tissues. When using macaque tracer-derived connections as the ground truth, we found that both global and local algorithms generated non-random patterns of false negative and false positive connections that were probably related to specific fiber systems and largely independent of the tractography algorithm or tissue type (post-mortem vs. in vivo) used in the current study. Moreover, a close examination of the transcallosal motor connections, reconstructed via either global or local tractography, demonstrated that the lateral transcallosal fibers in humans and macaques did not exhibit the denser homotopic connections found in primate tracer studies, indicating the need for more robust brain mapping techniques based on diffusion MRI data.
The neuropeptide oxytocin (OT) plays a critical role in modulating social behavior across a wide range of vertebrate species. In humans, intranasal oxytocin (INOT) has been shown to modulate various aspects of social behavior, such as empathy, trust, in-group preference, and memory of socially relevant cues. Most INOT studies employ cross-sectional designs despite the enhanced statistical power and reduction in error variance associated with individual differences characteristic of within-subject designs. Using the Prisoner Dilemma task, which models a real-life dyadic social interaction, our group has systematically explored the effect of INOT on social cooperation and non-cooperation using a cross-sectional design. In the current study, we investigated if the main findings from our cross-sectional study could be replicated in a within-subject design using the same paradigm and whether new findings would emerge. We found OT to attenuate the ventral tegmental area response to reciprocated cooperation in women, an effect that is also present in our cross-sectional sample. However, other cross-sectional findings, especially those found in men, were not observed in this within-subject study. We hypothesize that the discrepancy can be explained by differing OT effects based on the degree of stimulus novelty/familiarity. Our within-subject study also revealed new effects not found previously in our cross-sectional study. Most importantly, OT treatment on scan 2 blocked amygdala habituation to unreciprocated cooperation found in a group that received placebo on both scans among men. Our results suggest that exogenous OT reduces the salience of positive social interactions among women and prevents habituation to negative social interactions among men. These findings may have implications for the potential clinical utility of OT as a treatment for psychiatric disorders.
Our two closest living primate relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), exhibit significant behavioral differences despite belonging to the same genus and sharing a very recent common ancestor. Differences have been reported in multiple aspects of social behavior, including aggression, sex, play and cooperation. However, the neurobiological basis of these differences has only been minimally investigated and remains uncertain. Here, we present the first ever comparison of chimpanzee and bonobo brains using diffusion tensor imaging, supplemented with a voxel-wise analysis of T1-weighted images to specifically compare neural circuitry implicated in social cognition. We find that bonobos have more gray matter in brain regions involved in perceiving distress in both oneself and others, including the right dorsal amygdala and right anterior insula. Bonobos also have a larger pathway linking the amygdala with the ventral anterior cingulate cortex, a pathway implicated in both top–down control of aggressive impulses as well as bottom–up biases against harming others. We suggest that this neural system not only supports increased empathic sensitivity in bonobos, but also behaviors like sex and play that serve to dissipate tension, thereby limiting distress and anxiety to levels conducive with prosocial behavior.
The neural mechanisms supporting social bonds between adult men remain uncertain. In this double-blind, placebo-controlled study, we investigate the impact of intranasally administered oxytocin (OT) and vasopressin (AVP) on behavior and brain activity among men in the context of an iterated Prisoner’s Dilemma game, which models a real-life social situation. fMRI results show that, relative to both AVP and placebo, OT increases the caudate nucleus response to reciprocated cooperation, which may augment the reward of reciprocated cooperation and/or facilitate learning that another person can be trusted. OT also enhances left amygdala activation in response to reciprocated cooperation. Behaviorally, OT was associated with increased rates of cooperation following unreciprocated cooperation in the previous round compared with AVP. AVP strongly increased cooperation in response to a cooperative gesture by the partner compared with both placebo and OT. In response to reciprocated cooperation, AVP increased activation in a region spanning known vasopressin circuitry implicated in affiliative behaviors in other species. Finally, both OT and AVP increase amygdala functional connectivity with the anterior insula relative to placebo, which may increase the amygdala’s ability to elicit visceral somatic markers that guide decision making. These findings extend our knowledge of the neural and behavioral effects of OT and AVP to the context of genuine social interactions.
The evolution of neurocranial morphology in Homo sapiens is characterized by bulging of the parietal region, a feature unique to our species. In modern humans, expansion of the parietal surface occurs during the first year of life, in a morphogenetic stage which is absent in chimpanzees and Neandertals. A similar variation in brain shape among living adult humans is associated with expansion of the precuneus. Using MRI-derived structural brain templates, we compare medial brain morphology between humans and chimpanzees through shape analysis and geometrical modeling. We find that the main spatial difference is a prominent expansion of the precuneus in our species, providing further evidence of evolutionary changes associated with this area. The precuneus is a major hub of brain organization, a central node of the default-mode network, and plays an essential role in visuospatial integration. Together, the comparative neuroanatomical and paleontological evidence suggest that precuneus expansion is a neurological specialization of H. sapiens that evolved in the last 150,000 years that may be associated with recent human cognitive specializations.
Intranasal oxytocin (OT) can modulate social-emotional functioning and related brain activity in humans. Consequently, OT has been discussed as a potential treatment for psychiatric disorders involving social behavioral deficits. However, OT effects are often heterogeneous across individuals. Here we explore individual differences in OT effects on the neural response to social cooperation as a function of the rs53576 polymorphism of the oxytocin receptor gene (OXTR). Previously, we conducted a double-blind, placebo-controlled study in which healthy men and women were randomized to treatment with intranasal OT or placebo. Afterwards, they were imaged with functional magnetic resonance imaging while playing an iterated Prisoner's Dilemma Game with same-sex partners. Within the left ventral caudate nucleus, intranasal OT treatment increased activation to reciprocated cooperation in men, but tended to decrease activation in women. Here, we show that these sex differences in OT effects are specific to individuals with the rs53576 GG genotype, and are not found for other genotypes (rs53576 AA/AG). Thus, OT may increase the reward or salience of positive social interactions for male GG homozygotes, while decreasing those processes for female GG homozygotes. These results suggest that rs53576 genotype is an important variable to consider in future investigations of the clinical efficacy of intranasal OT treatment.
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.
Anxiety disorders are characterized by hyperactivity in both the amygdala and the anterior insula. Interventions that normalize activity in these areas may therefore be effective in treating anxiety disorders. Recently, there has been significant interest in the potential use of oxytocin (OT), as well as vasopressin (AVP) antagonists, as treatments for anxiety disorders. In this double-blind, placebo-controlled, pharmaco- fMRI study, 153 men and 151 women were randomized to treatment with either 24 IU intranasal OT, 20 IU intranasal AVP, or placebo and imaged with fMRI as they played the iterated Prisoner’s Dilemma game with same-sex human and computer partners. In men, OT attenuated the fMRI response to unreciprocated cooperation (CD), a negative social interaction, within the amygdala and anterior insula. This effect was specific to interactions with human partners. In contrast, among women, OT unexpectedly attenuated the amygdala and anterior insula response to unreciprocated cooperation from computer but not human partners. Among women, AVP did not significantly modulate the response to unreciprocated cooperation in either the amygdala or the anterior insula. However, among men, AVP attenuated the BOLD response to CD outcomes with human partners across a relatively large cluster including the amygdala and the anterior insula, which was contrary to expectations. Our results suggest that OT may decrease the stress of negative social interactions among men, whereas these effects were not found in women interacting with human partners. These findings support continued investigation into the possible efficacy of OT as a treatment for anxiety disorders.