Neuromorphological changes following selection for tameness and aggression in the Russian fox-farm experiment.

The Russian fox-farm experiment is an unusually long-running and well-controlled study designed to replicate wolf-to-dog domestication. As such, it offers an unprecedented window onto the neural mechanisms governing the evolution of behavior. Here we report evolved changes to gray matter morphology resulting from selection for tameness vs. aggressive responses toward humans in a sample of 30 male fox brains. Contrasting with standing ideas on the effects of domestication on brain size, tame foxes did not show reduced brain volume. Rather, gray matter volume in both the tame and aggressive strains was increased relative to conventional farm foxes bred without deliberate selection on behavior. Furthermore, tame- and aggressive-enlarged regions overlapped substantially, including portions of motor, somatosensory, and prefrontal cortex, amygdala, hippocampus, and cerebellum. We also observed differential morphological covariation across distributed gray matter networks. In one prefrontal-cerebellum network, this covariation differentiated the three populations along the tame-aggressive behavioral axis. Surprisingly, a prefrontal-hypothalamic network differentiated the tame and aggressive foxes together from the conventional strain. These findings indicate that selection for opposite behaviors can influence brain morphology in a similar way.SIGNIFICANCE STATEMENTDomestication represents one of the largest and most rapid evolutionary shifts of life on earth. However, its neural correlates are largely unknown. Here we report the neuroanatomical consequences of selective breeding for tameness or aggression in the seminal Russian fox-farm experiment. Compared to a population of conventional farm-bred control foxes, tame foxes show neuroanatomical changes in the prefrontal cortex and hypothalamus, paralleling wolf-to-dog shifts. Surprisingly, though, aggressive foxes also show similar changes. Moreover, both strains show increased gray matter volume relative to controls. These results indicate that similar brain adaptations can result from selection for opposite behavior, that existing ideas of brain changes in domestication may need revision, and that significant neuroanatomical change can evolve very quickly - within the span of less than a hundred generations.

White matter pathways associated with empathy in females: A DTI investigation.

Empathy is a component of social cognition that allows us to understand, perceive, experience, and respond to the emotional state of others. In this study, we seek to build on previous research that suggests that sex and hormone levels may impact white matter microstructure. These white matter microstructural differences may influence social cognition. We examine the fractional anisotropy (FA) of white matter pathways associated with the complex human process of empathy in healthy young adult females during the self-reported luteal phase of their menstrual cycle. We used tract-based spatial statistics to perform statistical comparisons of FA and conducted multiple linear regression analysis to examine the strength of association between white matter FA and scores on the Empathy Quotient (EQ), a self-report questionnaire in which individuals report how much they agree or disagree with 60 statements pertaining to their empathic tendencies. Results identified a significant negative relationship between EQ scores and FA within five clusters of white matter: in the left forceps minor/body of the corpus callosum, left corticospinal tract, intraparietal sulcus/primary somatosensory cortex, superior longitudinal fasciculus, and right inferior fronto-occipital fasciculus/forceps minor. These consistent findings across clusters suggest that lower self-reported empathy is related to higher FA across healthy young females in specific white matter regions during the menstrual luteal phase. Future research should seek to examine if self-reported empathy varies across the menstrual cycle, using blood samples to confirm cycle phase and hormone levels.

Imaging evolution of the primate brain: the next frontier?

Evolution, as we currently understand it, strikes a delicate balance between animals' ancestral history and adaptations to their current niche. Similarities between species are generally considered inherited from a common ancestor whereas observed differences are considered as more recent evolution. Hence comparing species can provide insights into the evolutionary history. Comparative neuroimaging has recently emerged as a novel subdiscipline, which uses magnetic resonance imaging (MRI) to identify similarities and differences in brain structure and function across species. Whereas invasive histological and molecular techniques are superior in spatial resolution, they are laborious, post-mortem, and oftentimes limited to specific species. Neuroimaging, by comparison, has the advantages of being applicable across species and allows for fast, whole-brain, repeatable, and multi-modal measurements of the structure and function in living brains and post-mortem tissue. In this review, we summarise the current state of the art in comparative anatomy and function of the brain and gather together the main scientific questions to be explored in the future of the fascinating new field of brain evolution derived from comparative neuroimaging.

Significant Neuroanatomical Variation Among Domestic Dog Breeds.

Humans have bred different lineages of domestic dogs for different tasks such as hunting, herding, guarding, or companionship. These behavioral differences must be the result of underlying neural differences, but surprisingly, this topic has gone largely unexplored. The current study examined whether and how selective breeding by humans has altered the gross organization of the brain in dogs. We assessed regional volumetric variation in MRI studies of 62 male and female dogs of 33 breeds. Neuroanatomical variation is plainly visible across breeds. This variation is distributed nonrandomly across the brain. A whole-brain, data-driven independent components analysis established that specific regional subnetworks covary significantly with each other. Variation in these networks is not simply the result of variation in total brain size, total body size, or skull shape. Furthermore, the anatomy of these networks correlates significantly with different behavioral specialization(s) such as sight hunting, scent hunting, guarding, and companionship. Importantly, a phylogenetic analysis revealed that most change has occurred in the terminal branches of the dog phylogenetic tree, indicating strong, recent selection in individual breeds. Together, these results establish that brain anatomy varies significantly in dogs, likely due to human-applied selection for behavior.SIGNIFICANCE STATEMENT Dog breeds are known to vary in cognition, temperament, and behavior, but the neural origins of this variation are unknown. In an MRI-based analysis, we found that brain anatomy covaries significantly with behavioral specializations such as sight hunting, scent hunting, guarding, and companionship. Neuroanatomical variation is not simply driven by brain size, body size, or skull shape, and is focused in specific networks of regions. Nearly all of the identified variation occurs in the terminal branches of the dog phylogenetic tree, indicating strong, recent selection in individual breeds. These results indicate that through selective breeding, humans have significantly altered the brains of different lineages of domestic dogs in different ways.

A novel social attribution paradigm: The Dynamic Interacting Shape Clips (DISC).

The Dynamic Interacting Shape Clips (DISC) is a novel stimulus set designed to examine mentalizing, specifically social attribution, suitable for use with diverse methodologies including fMRI. The DISC offer some advantages compared to other social attribution stimuli including a large number of stimuli, subsets of stimuli depicting different kinds of social interactions (i.e., friendly approach, aggression, and avoidance), and two control tasks-one that contrasts interpretations of socially contingent movement versus random, inanimate movement, and the other that examines the impact of attentional shifts on mentalizing using the same visual stimuli with a different cue. This study describes both behavioral and fMRI findings from a sample of 22 typically developing adults (mage = 21.7 years, SD = 1.72). Behavioral data supports participants anthropomorphized the stimuli and the social intent of the clips were perceived as intended. Neuroimaging findings demonstrate that brain areas associated with processing animacy and mental state attribution were activated when participants were shown clips featuring social interactions compared to random movement, and when attention was cued to social versus physical aspects of the same stimuli. Results lend empirical support for the use of the DISC in future studies of social cognition.

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.

SIPsmartER delivered through rural, local health districts: adoption and implementation outcomes.

BACKGROUND: SIPsmartER is a 6-month evidenced-based, multi-component behavioral intervention that targets sugar-sweetened beverages among adults. It consists of three in-person group classes, one teach-back call, and 11 automated phone calls. Given SIPsmartER's previously demonstrated effectiveness, understanding its adoption, implementation, and potential for integration within a system that reaches health disparate communities is important to enhance its public health impact. During this pilot dissemination and implementation trial, SIPsmartER was delivered by trained staff from local health districts (delivery agents) in rural, Appalachian Virginia. SIPsmartER's execution was supported by consultee-centered implementation strategies. METHODS: In this mixed-methods process evaluation, adoption and implementation indicators of the program and its implementation strategy (e.g., fidelity, feasibility, appropriateness, acceptability) were measured using tracking logs, delivery agent surveys and interviews, and fidelity checklists. Quantitative data were analyzed with descriptive statistics. Qualitative data were inductively coded. RESULTS: Delivery agents implemented SIPsmartER to the expected number of cohorts (n = 12), recruited 89% of cohorts, and taught 86% of expected small group classes with > 90% fidelity. The planned implementation strategies were also executed with high fidelity. Delivery agents completing the two-day training, pre-lesson meetings, fidelity checklists, and post-lesson meetings at rates of 86, 75, 100, and 100%, respectively. Additionally, delivery agents completed 5% (n = 3 of 66) and 10% (n = 6 of 59) of teach-back and missed class calls, respectively. On survey items using 6-point scales, delivery agents reported, on average, higher feasibility, appropriateness, and acceptability related to delivering the group classes (range 4.3 to 5.6) than executing missed class and teach-back calls (range 2.6 to 4.6). They also, on average, found the implementation strategy activities to be helpful (range 4.9 to 6.0). Delivery agents identified strengths and weakness related to recruitment, lesson delivery, call completion, and the implementation strategy. CONCLUSIONS: In-person classes and the consultee-centered implementation strategies were viewed as acceptable, appropriate, and feasible and were executed with high fidelity. However, implementation outcomes for teach-back and missed class calls and recruitment were not as strong. Findings will inform the future full-scale dissemination and implementation of SIPsmartER, as well as other evidence-based interventions, into rural health districts as a means to improve population health.

A Participatory Process to Engage Appalachian Youth in Reducing Sugar-Sweetened Beverage Consumption.

Children and adolescents consume excessive amounts of sugar-sweetened beverages (SSBs), which are associated with adverse health outcomes. We describe a yearlong participatory research study to reduce SSBs in Central Appalachia, where excessive consumption is particularly prevalent. This study was conducted in partnership with a community advisory board in Southwest Virginia. Nine "youth ambassadors," aged 10 to 13 years helped to systematically adapt SIPsmartER, an effective theory-based program for Appalachian adults, to be age and culturally appropriate and meet desired theoretical objectives. They then assisted with delivering the curriculum during a school-based feasibility study and led an advocacy event in their community. Satisfaction surveys and feedback sessions indicate that ambassadors found the program acceptable and important for other students. Validated surveys and focus groups suggested that theoretical objectives were met. Findings from these mixed methods sources informed curricular changes to further enhance acceptability and refine theoretical objectives. Participation in follow-up advocacy activities was tracked and described. Following the yearlong study, ambassadors reported having advocacy skills and motivation to continue reducing SSB intake in their community. Results, challenges, and lessons learned are presented to inform larger efforts to enhance acceptability of programs and inspire youth to take action to reduce health disparities in Appalachian communities.

Intranasal oxytocin in rhesus monkeys alters brain networks that detect social salience and reward.

In primates, resting state functional neuroimaging (rsfcMRI) has identified several large-scale, intrinsic brain networks, including the salience network (SN), which is involved in detecting stimulus salience. Intranasal oxytocin (IN-OT) has been shown to modulate the salience and rewarding quality of social stimuli in mammals and numerous studies have shown that it can affect the functional connectivity between brain regions. Less is known, however, about how these effects unfold over time following IN-OT administration. This study used rsfcMRI in anesthetized rhesus macaques to track temporal changes in the functional connectivity between brain regions involved in the SN, including the anterior cingulate cortex (ACC), anterior insula (AI), amygdala (amy), and ventral striatum (vstr), lasting 3 hr after IN-OT or Placebo (saline) administration. We found significant temporal changes in the functional connectivity between all regions associated with treatment condition. IN-OT increased the functional connectivity between AI_vstr, ACC_amy (right hemisphere), ACC_vstr (left hemisphere), and amy_vstr (right hemisphere), but reduced the functional connectivity between ACC_AI, and the AI_amygdala. These results suggest that IN-OT may dampen salience detection in rhesus monkeys, consistent with previous findings of reduced social vigilance, while enhancing the connectivity between the SN and regions involved in processing reward.

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

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.

Associations between autistic traits and fractional anisotropy values in white matter tracts in a nonclinical sample of young adults.

Whereas a number of studies have examined relationships among brain activity, social cognitive skills, and autistic traits, fewer studies have evaluated whether structural connections among brain regions relate to these traits and skills. Uncinate fasciculus (UF) and inferior longitudinal fasciculus (ILF) are white matter tracts that may underpin the behavioral expression of these skills because they connect regions within or provide sensory information to brain areas implicated in social cognition, and structural differences in these tracts have been associated with autistic traits. We examined relationships among self-reported autistic traits, mentalizing, and water diffusivity in UF and ILF in a nonclinical sample of 24 young adults (mean age = 21.92 years, SD = 4.72 years; 15 women). We measured autistic traits using the Autism-Spectrum Quotient, and we measured mentalizing using the Dynamic Interactive Shapes Clips task. We used Tract-Based Spatial Statistics and randomize to examine relationships among fractional anisotropy (FA) values in bilateral ILF and UF, age, cognitive abilities, autistic traits, and mentalizing. Autistic traits were positively related to FA values in left ILF. No other relationships between FA values and other variables were significant. Results suggest that left ILF may be involved in the expression of autistic traits in individuals without clinical diagnoses.

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.

A comparative analysis of mouse and human medial geniculate nucleus connectivity: a DTI and anterograde tracing study.

Understanding the function and connectivity of thalamic nuclei is critical for understanding normal and pathological brain function. The medial geniculate nucleus (MGN) has been studied mostly in the context of auditory processing and its connection to the auditory cortex. However, there is a growing body of evidence that the MGN and surrounding associated areas ('MGN/S') have a diversity of projections including those to the globus pallidus, caudate/putamen, amygdala, hypothalamus, and thalamus. Concomitantly, pathways projecting to the medial geniculate include not only the inferior colliculus but also the auditory cortex, insula, cerebellum, and globus pallidus. Here we expand our understanding of the connectivity of the MGN/S by using comparative diffusion weighted imaging with probabilistic tractography in both human and mouse brains (most previous work was in rats). In doing so, we provide the first report that attempts to match probabilistic tractography results between human and mice. Additionally, we provide anterograde tracing results for the mouse brain, which corroborate the probabilistic tractography findings. Overall, the study provides evidence for the homology of MGN/S patterns of connectivity across species for understanding translational approaches to thalamic connectivity and function. Further, it points to the utility of DTI in both human studies and small animal modeling, and it suggests potential roles of these connections in human cognition, behavior, and disease.

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 Grauer's 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.

Differences in neural activation for object-directed grasping in chimpanzees and humans.

The human faculty for object-mediated action, including tool use and imitation, exceeds that of even our closest primate relatives and is a key foundation of human cognitive and cultural uniqueness. In humans and macaques, observing object-directed grasping actions activates a network of frontal, parietal, and occipitotemporal brain regions, but differences in human and macaque activation suggest that this system has been a focus of selection in the primate lineage. To study the evolution of this system, we performed functional neuroimaging in humans' closest living relatives, chimpanzees. We compare activations during performance of an object-directed manual grasping action, observation of the same action, and observation of a mimed version of the action that consisted of only movements without results. Performance and observation of the same action activated a distributed frontoparietal network similar to that reported in macaques and humans. Like humans and unlike macaques, these regions were also activated by observing movements without results. However, in a direct chimpanzee/human comparison, we also identified unique aspects of human neural responses to observed grasping. Chimpanzee activation showed a prefrontal bias, including significantly more activity in ventrolateral prefrontal cortex, whereas human activation was more evenly distributed across more posterior regions, including significantly more activation in ventral premotor cortex, inferior parietal cortex, and inferotemporal cortex. This indicates a more "bottom-up" representation of observed action in the human brain and suggests that the evolution of tool use, social learning, and cumulative culture may have involved modifications of frontoparietal interactions.

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.

NSF workshop report: discovering general principles of nervous system organization by comparing brain maps across species.

Efforts to understand nervous system structure and function have received new impetus from the federal Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Initiative. Comparative analyses can contribute to this effort by leading to the discovery of general principles of neural circuit design, information processing, and gene-structure-function relationships that are not apparent from studies on single species. We here propose to extend the comparative approach to nervous system 'maps' comprising molecular, anatomical, and physiological data. This research will identify which neural features are likely to generalize across species, and which are unlikely to be broadly conserved. It will also suggest causal relationships between genes, development, adult anatomy, physiology, and, ultimately, behavior. These causal hypotheses can then be tested experimentally. Finally, insights from comparative research can inspire and guide technological development. To promote this research agenda, we recommend that teams of investigators coalesce around specific research questions and select a set of 'reference species' to anchor their comparative analyses. These reference species should be chosen not just for practical advantages, but also with regard for their phylogenetic position, behavioral repertoire, well-annotated genome, or other strategic reasons. We envision that the nervous systems of these reference species will be mapped in more detail than those of other species. The collected data may range from the molecular to the behavioral, depending on the research question. To integrate across levels of analysis and across species, standards for data collection, annotation, archiving, and distribution must be developed and respected. To that end, it will help to form networks or consortia of researchers and centers for science, technology, and education that focus on organized data collection, distribution, and training. These activities could be supported, at least in part, through existing mechanisms at NSF, NIH, and other agencies. It will also be important to develop new integrated software and database systems for cross-species data analyses. Multidisciplinary efforts to develop such analytical tools should be supported financially. Finally, training opportunities should be created to stimulate multidisciplinary, integrative research into brain structure, function, and evolution.

Covariation of Skull and Brain Morphology in Domestic Dogs.

Despite their distinct embryonic origins, the skull and brain are highly integrated. Understanding the covariation between the skull and brain can shed light on anatomical, cognitive, and behavioral traits in extant and extinct species. Domestic dogs offer a unique opportunity to investigate skull-brain covariation due to their diverse skull morphologies and neural anatomy. To assess this question, we examined T2-weighted MRI studies of 62 dogs from 33 breeds, plus an additional 17 dogs of mixed or unknown breeds. Scans were opportunistically collected from a veterinary teaching hospital of dogs that were referred for neurological examination but did not have grossly observable structural brain abnormalities. As the neurocrania of dogs become broader and shorter, there is a significant decrease in the gray matter volume of the right olfactory bulb, frontal cortex, marginal gyrus, and cerebellum. On the other hand, as the neurocrania of dogs become narrower and longer, there is a significant decrease in the gray matter volume of the olfactory bulb, frontal cortex, temporal cortex, amygdala, hypothalamus, hippocampus, periaqueductal gray, cerebellum, and brainstem. Selective breeding for specific skull shapes may impact canine brain anatomy and function.

A prominent vertical occipital white matter fasciculus unique to primate brains.

Vision in humans and other primates enlists parallel processing streams in the dorsal and ventral visual cortex, known to support spatial and object processing, respectively. These streams are bridged, however, by a prominent white matter tract, the vertical occipital fasciculus (VOF), identified in both classical neuroanatomy and recent diffusion-weighted magnetic resonance imaging (dMRI) studies. Understanding the evolution of the VOF may shed light on its origin, function, and role in visually guided behaviors. To this end, we acquired high-resolution dMRI data from the brains of select mammalian species, including anthropoid and strepsirrhine primates, a tree shrew, rodents, and carnivores. In each species, we attempted to delineate the VOF after first locating the optic radiations in the occipital white matter. In all primate species examined, the optic radiation was flanked laterally by a prominent and coherent white matter fasciculus recognizable as the VOF. By contrast, the equivalent analysis applied to four non-primate species from the same superorder as primates (tree shrew, ground squirrel, paca, and rat) failed to reveal white matter tracts in the equivalent location. Clear evidence for a VOF was also absent in two larger carnivore species (ferret and fox). Although we cannot rule out the existence of minor or differently organized homologous fiber pathways in the non-primate species, the results suggest that the VOF has greatly expanded, or possibly emerged, in the primate lineage. This adaptation likely facilitated the evolution of unique visually guided behaviors in primates, with direct impacts on manual object manipulation, social interactions, and arboreal locomotion.

Fermentation technology as a driver of human brain expansion.

Brain tissue is metabolically expensive. Consequently, the evolution of humans' large brains must have occurred via concomitant shifts in energy expenditure and intake. Proposed mechanisms include dietary shifts such as cooking. Importantly, though, any new food source must have been exploitable by hominids with brains a third the size of modern humans'. Here, we propose the initial metabolic trigger of hominid brain expansion was the consumption of externally fermented foods. We define "external fermentation" as occurring outside the body, as opposed to the internal fermentation in the gut. External fermentation could increase the bioavailability of macro- and micronutrients while reducing digestive energy expenditure and is supported by the relative reduction of the human colon. We discuss the explanatory power of our hypothesis and survey external fermentation practices across human cultures to demonstrate its viability across a range of environments and food sources. We close with suggestions for empirical tests.