Evolutionary adaptations of the human brain are the basis for our unique abilities such as language. An expansion of the arcuate fasciculus (AF), the dorsal language tract, in the human lineage ...involving left lateralization is considered canonical, but this hypothesis has not been tested in relation to other architectural adaptations in the human brain. Using diffusion-weighted MRI, we examined AF in the human and macaque and quantified species differences in white matter architecture and surface representations. To compare surface results in the two species, we transformed macaque representations to human space using a landmark-based monkey-to-human cortical expansion model.
We found that the human dorsal AF, but not the ventral inferior fronto-occipital fasciculus (IFO), is left-lateralized. In the monkey AF is not lateralized. Moreover, compared to the macaque, human AF is relatively increased with respect to IFO. A comparison of human and transformed macaque surface representations suggests that cortical expansion alone cannot account for the species differences in the surface representation of AF.
Our results show that the human AF has undergone critical anatomical modifications in comparison with the macaque AF. More generally, this work demonstrates that studies on the human brain specializations underlying the language connectome can benefit from current methodological advances in comparative neuroanatomy.
Comparing the brains of related species faces the challenges of establishing homologies whilst accommodating evolutionary specializations. Here we propose a general framework for understanding ...similarities and differences between the brains of primates. The approach uses white matter blueprints of the whole cortex based on a set of white matter tracts that can be anatomically matched across species. The blueprints provide a common reference space that allows us to navigate between brains of different species, identify homologous cortical areas, or to transform whole cortical maps from one species to the other. Specializations are cast within this framework as deviations between the species' blueprints. We illustrate how this approach can be used to compare human and macaque brains.
Abstract Adaptive information seeking is essential for humans to effectively navigate complex and dynamic environments. Here, we developed a gaze-contingent eye-tracking paradigm to examine the early ...emergence of adaptive information-seeking. Toddlers ( N = 60, 18-36 months) and adults ( N = 42) either learnt that an animal was equally likely to be found in any of four available locations, or that it was most likely to be found in one particular location. Afterwards, they were given control of a torchlight, which they could move with their eyes to explore the otherwise pitch-black task environment. Eye-movement data and Markov models show that, from 24 months of age, toddlers become more exploratory than adults, and start adapting their exploratory strategies to the information structure of the task. These results show that toddlers’ search strategies are more sophisticated than previously thought, and identify the unique features that distinguish their information search from adults’.
Diffusion magnetic resonance imaging (dMRI) is commonly used to assess the tissue and cellular substructure of the human brain. In the white matter, myelinated axons are the principal neural elements ...that shape dMRI through the restriction of water diffusion; however, in the gray matter the relative contributions of myelinated axons and other tissue features to dMRI are poorly understood. Here we investigate the determinants of diffusion in the cerebral cortex. Specifically, we ask whether myelinated axons significantly shape dMRI fractional anisotropy (dMRI-FA), a measure commonly used to characterize tissue properties in humans. We compared ultra-high resolution ex vivo dMRI data from the brain of a marmoset monkey with both myelin- and Nissl-stained histological sections obtained from the same brain after scanning. We found that the dMRI-FA did not match the spatial distribution of myelin in the gray matter. Instead dMRI-FA was more closely related to the anisotropy of stained tissue features, most prominently those revealed by Nissl staining and to a lesser extent those revealed by myelin staining. Our results suggest that unmyelinated neurites such as large caliber apical dendrites are the primary features shaping dMRI measures in the cerebral cortex.
Abstract
The human cingulate sulcus visual area (CSv) responds selectively to visual and vestibular cues to self-motion. Although it is more selective for visual self-motion cues than any other brain ...region studied, it is not known whether CSv mediates perception of self-motion. An alternative hypothesis, based on its location, is that it provides sensory information to the motor system for use in guiding locomotion. To evaluate this hypothesis we studied the connectivity pattern of CSv, which is completely unknown, with a combination of diffusion MRI and resting-state functional MRI. Converging results from the 2 approaches suggest that visual drive is provided primarily by areas hV6, pVIP (putative intraparietal cortex) and PIC (posterior insular cortex). A strong connection with the medial portion of the somatosensory cortex, which represents the legs and feet, suggests that CSv may receive locomotion-relevant proprioceptive information as well as visual and vestibular signals. However, the dominant connections of CSv are with specific components of the motor system, in particular the cingulate motor areas and the supplementary motor area. We propose that CSv may provide a previously unknown link between perception and action that serves the online control of locomotion.
•Advances in primate neuroimaging enable comparative connectomics.•The number of cortical neurons and size of social group are associated in non-human primates.•Resting-state and hyperscanning fMRI ...enable static and dynamic investigations to social functions, respectively.•Ventral premotor and default mode networks exhibits homologous functional organization in human and macaque.•Modular differentiation hypothesis for inferior parietal lobule linked to social behavior.
Social interaction is thought to provide a selection pressure for human intelligence, yet little is known about its neurobiological basis and evolution throughout the primate lineage. Recent advances in neuroimaging have enabled whole brain investigation of brain structure, function, and connectivity in humans and non-human primates (NHPs), leading to a nascent field of comparative connectomics. However, linking social behavior to brain organization across the primates remains challenging. Here, we review the current understanding of the macroscale neural mechanisms of social behaviors from the viewpoint of system neuroscience. We first demonstrate an association between the number of cortical neurons and the size of social groups across primates, suggesting a link between neural information-processing capacity and social capabilities. Moreover, by capitalizing on recent advances in species-harmonized functional MRI, we demonstrate that portions of the mirror neuron system and default-mode networks, which are thought to be important for representation of the other's actions and sense of self, respectively, exhibit similarities in functional organization in macaque monkeys and humans, suggesting possible homologies. With respect to these two networks, we describe recent developments in the neurobiology of social perception, joint attention, personality and social complexity. Together, the Human Connectome Project (HCP)-style comparative neuroimaging, hyperscanning, behavioral, and other multi-modal investigations are expected to yield important insights into the evolutionary foundations of human social behavior.
Despite widespread interest in social dominance, little is known of its neural correlates in primates. We hypothesized that social status in primates might be related to individual variation in ...subcortical brain regions implicated in other aspects of social and emotional behavior in other mammals. To examine this possibility we used magnetic resonance imaging (MRI), which affords the taking of quantitative measurements noninvasively, both of brain structure and of brain function, across many regions simultaneously. We carried out a series of tests of structural and functional MRI (fMRI) data in 25 group-living macaques. First, a deformation-based morphometric (DBM) approach was used to show that gray matter in the amygdala, brainstem in the vicinity of the raphe nucleus, and reticular formation, hypothalamus, and septum/striatum of the left hemisphere was correlated with social status. Second, similar correlations were found in the same areas in the other hemisphere. Third, similar correlations were found in a second data set acquired several months later from a subset of the same animals. Fourth, the strength of coupling between fMRI-measured activity in the same areas was correlated with social status. The network of subcortical areas, however, had no relationship with the sizes of individuals' social networks, suggesting the areas had a simple and direct relationship with social status. By contrast a second circuit in cortex, comprising the midsuperior temporal sulcus and anterior and dorsal prefrontal cortex, covaried with both individuals' social statuses and the social network sizes they experienced. This cortical circuit may be linked to the social cognitive processes that are taxed by life in more complex social networks and that must also be used if an animal is to achieve a high social status.
Traditional theories frame curiosity as an intrinsic motivation to obtain information to resolve uncertainty.Recent empirical breakthroughs challenge this perspective and reframe curiosity in terms ...of the learning process itself: curiosity is sustained when individuals perceive improvements in their performance and actively engage in the process of learning.Unlike previous research, which remained agnostic about the change of curiosity over time, the learning progress framework provides insights into the temporal dynamics of curiosity, shedding light on its fluctuations based on the extent of learning progress individuals make.By integrating the desire to obtain information with the drive to make learning progress, we offer a unified account of curiosity.
What drives our curiosity remains an elusive and hotly debated issue, with multiple hypotheses proposed but a cohesive account yet to be established. This review discusses traditional and emergent theories that frame curiosity as a desire to know and a drive to learn, respectively. We adopt a model-based approach that maps the temporal dynamics of various factors underlying curiosity-based exploration, such as uncertainty, information gain, and learning progress. In so doing, we identify the limitations of past theories and posit an integrated account that harnesses their strengths in describing curiosity as a tool for optimal environmental exploration. In our unified account, curiosity serves as a ‘common currency’ for exploration, which must be balanced with other drives such as safety and hunger to achieve efficient action.
What drives our curiosity remains an elusive and hotly debated issue, with multiple hypotheses proposed but a cohesive account yet to be established. This review discusses traditional and emergent theories that frame curiosity as a desire to know and a drive to learn, respectively. We adopt a model-based approach that maps the temporal dynamics of various factors underlying curiosity-based exploration, such as uncertainty, information gain, and learning progress. In so doing, we identify the limitations of past theories and posit an integrated account that harnesses their strengths in describing curiosity as a tool for optimal environmental exploration. In our unified account, curiosity serves as a ‘common currency’ for exploration, which must be balanced with other drives such as safety and hunger to achieve efficient action.
Comparative neuroscience is entering the era of big data. New high-throughput methods and data-sharing initiatives have resulted in the availability of large, digital data sets containing many types ...of data from ever more species. Here, we present a framework for exploiting the new possibilities offered. The multimodality of the data allows vertical translations, which are comparisons of different aspects of brain organization within a single species and across scales. Horizontal translations compare particular aspects of brain organization across species, often by building abstract feature spaces. Combining vertical and horizontal translations allows for more sophisticated comparisons, including relating principles of brain organization across species by contrasting horizontal translations, and for making formal predictions of unobtainable data based on observed results in a model species.
•Human and macaque temporal cortex share two principles of organisation.•Amongst other metrics, human’s temporal cortex processing capacity is significantly larger than that of other primates; ...connectivity of the temporal lobe shows elaboration in particular primate lineages.•Human temporal cortex also shows a distinct organization centred around expanded arcuate fascicle projections.•Many human abilities, including semantic processing, can be interpreted as elaborations and recycling of skills present in their common ancestor with other primates.
Temporal cortex is a primate specialization that shows considerable variation in size, morphology, and connectivity across species. Human temporal cortex is involved in many behaviors that are considered especially well developed in humans, including semantic processing, language, and theory of mind. Here, we ask whether the involvement of temporal cortex in these behaviors can be explained in the context of the ‘general’ primate organization of the temporal lobe or whether the human temporal lobe contains unique specializations indicative of a ‘step change’ in the lineage leading to modern humans. We propose that many human behaviors can be explained as elaborations of temporal cortex functions observed in other primates. However, changes in temporal lobe white matter suggest increased integration of information within temporal cortex and between posterior temporal cortex and other association areas, which likely enable behaviors not possible in other species.
PDF
