Navigation of brain networks

Understanding the mechanisms of neural communication in large-scale brain networks remains a major goal in neuroscience. We investigated whether navigation is a parsimonious routing model for connectomics. Navigating a network involves progressing to the next node that is closest in distance to a desired destination. We developed a measure to quantify navigation efficiency and found that connectomes in a range of mammalian species (human, mouse and macaque) can be successfully navigated with near-optimal efficiency (>80% of optimal efficiency for typical connection densities). Rewiring network topology or repositioning network nodes resulted in 45%-60% reductions in navigation performance. Specifically, we found that brain networks cannot be progressively rewired (randomized or clusterized) to result in topologies with significantly improved navigation performance. Navigation was also found to: i) promote a resource-efficient distribution of the information traffic load, potentially relieving communication bottlenecks; and, ii) explain significant variation in functional connectivity. Unlike prevalently studied communication strategies in connectomics, navigation does not mandate biologically unrealistic assumptions about global knowledge of network topology. We conclude that the wiring and spatial embedding of brain networks is conducive to effective decentralized communication. Graph-theoretic studies of the connectome should consider measures of network efficiency and centrality that are consistent with decentralized models of neural communication

Dwelling Quietly in the Rich Club: Brain Network Determinants of Slow Cortical Fluctuations

For more than a century, cerebral cartography has been driven by investigations of structural and morphological properties of the brain across spatial scales and the temporal/functional phenomena that emerge from these underlying features. The next era of brain mapping will be driven by studies that consider both of these components of brain organization simultaneously -- elucidating their interactions and dependencies. Using this guiding principle, we explored the origin of slowly fluctuating patterns of synchronization within the topological core of brain regions known as the rich club, implicated in the regulation of mood and introspection. We find that a constellation of densely interconnected regions that constitute the rich club (including the anterior insula, amygdala, and precuneus) play a central role in promoting a stable, dynamical core of spontaneous activity in the primate cortex. The slow time scales are well matched to the regulation of internal visceral states, corresponding to the somatic correlates of mood and anxiety. In contrast, the topology of the surrounding "feeder" cortical regions show unstable, rapidly fluctuating dynamics likely crucial for fast perceptual processes. We discuss these findings in relation to psychiatric disorders and the future of connectomics.Comment: 35 pages, 6 figure

Resting-state connectivity and functional specialization in human medial parieto-occipital cortex

According to recent models of visuo-spatial processing, the medial parieto-occipital cortex is a crucial node of the dorsal visual stream. Evidence from neurophysiological studies in monkeys has indicated that the parieto-occipital sulcus (POS) contains three functionally and cytoarchitectonically distinct areas: the visual area V6 in the fundus of the POS, and the visuo-motor areas V6Av and V6Ad in a progressively dorsal and anterior location with respect to V6. Besides different topographical organization, cytoarchitectonics, and functional properties, these three monkey areas can also be distinguished based on their patterns of cortico-cortical connections. Thanks to wide-field retinotopic mapping, areas V6 and V6Av have been also mapped in the human brain. Here, using a combined approach of resting-state functional connectivity and task-evoked activity by fMRI, we identified a new region in the anterior POS showing a pattern of functional properties and cortical connections that suggests a homology with the monkey area V6Ad. In addition, we observed distinct patterns of cortical connections associated with the human V6 and V6Av which are remarkably consistent with those showed by the anatomical tracing studies in the corresponding monkey areas. Consistent with recent models on visuo-spatial processing, our findings demonstrate a gradient of functional specialization and cortical connections within the human POS, with more posterior regions primarily dedicated to the analysis of visual attributes useful for spatial navigation and more anterior regions primarily dedicated to analyses of spatial information relevant for goal-directed action

Perspective: network-guided pattern formation of neural dynamics

The understanding of neural activity patterns is fundamentally linked to an understanding of how the brain's network architecture shapes dynamical processes. Established approaches rely mostly on deviations of a given network from certain classes of random graphs. Hypotheses about the supposed role of prominent topological features (for instance, the roles of modularity, network motifs, or hierarchical network organization) are derived from these deviations. An alternative strategy could be to study deviations of network architectures from regular graphs (rings, lattices) and consider the implications of such deviations for self-organized dynamic patterns on the network. Following this strategy, we draw on the theory of spatiotemporal pattern formation and propose a novel perspective for analyzing dynamics on networks, by evaluating how the self-organized dynamics are confined by network architecture to a small set of permissible collective states. In particular, we discuss the role of prominent topological features of brain connectivity, such as hubs, modules and hierarchy, in shaping activity patterns. We illustrate the notion of network-guided pattern formation with numerical simulations and outline how it can facilitate the understanding of neural dynamics

The specificity and robustness of long-distance connections in weighted, interareal connectomes

Brain areas' functional repertoires are shaped by their incoming and outgoing structural connections. In empirically measured networks, most connections are short, reflecting spatial and energetic constraints. Nonetheless, a small number of connections span long distances, consistent with the notion that the functionality of these connections must outweigh their cost. While the precise function of these long-distance connections is not known, the leading hypothesis is that they act to reduce the topological distance between brain areas and facilitate efficient interareal communication. However, this hypothesis implies a non-specificity of long-distance connections that we contend is unlikely. Instead, we propose that long-distance connections serve to diversify brain areas' inputs and outputs, thereby promoting complex dynamics. Through analysis of five interareal network datasets, we show that long-distance connections play only minor roles in reducing average interareal topological distance. In contrast, areas' long-distance and short-range neighbors exhibit marked differences in their connectivity profiles, suggesting that long-distance connections enhance dissimilarity between regional inputs and outputs. Next, we show that -- in isolation -- areas' long-distance connectivity profiles exhibit non-random levels of similarity, suggesting that the communication pathways formed by long connections exhibit redundancies that may serve to promote robustness. Finally, we use a linearization of Wilson-Cowan dynamics to simulate the covariance structure of neural activity and show that in the absence of long-distance connections, a common measure of functional diversity decreases. Collectively, our findings suggest that long-distance connections are necessary for supporting diverse and complex brain dynamics.Comment: 18 pages, 8 figure

Characterization of the Community Structure of Large Scale Functional Brain Networks During Ketamine-Medetomidine Anesthetic Induction

One of the central questions in neuroscience is to understand the way communication is organized in the brain, trying to comprehend how cognitive capacities or physiological states of the organism are potentially related to brain activities involving interactions of several brain areas. One important characteristic of the functional brain networks is that they are modularly structured, being this modular architecture regarded to account for a series of properties and functional dynamics. In the neurobiological context, communities may indicate brain regions that are involved in one same activity, representing neural segregated processes. Several studies have demonstrated the modular character of organization of brain activities. However, empirical evidences regarding to its dynamics and relation to different levels of consciousness have not been reported yet. Within this context, this research sought to characterize the community structure of functional brain networks during an anesthetic induction process. The experiment was based on intra-cranial recordings of neural activities of an old world macaque of the species Macaca fuscata during a Ketamine-Medetomidine anesthetic induction process. Networks were serially estimated in time intervals of five seconds. Changes were observed within about one and a half minutes after the administration of the anesthetics, revealing the occurrence of a transition on the community structure. The awake state was characterized by the presence of large clusters involving frontal and parietal regions, while the anesthetized state by the presence of communities in the primary visual and motor cortices, being the areas of the secondary associative cortex most affected. The results report the influence of general anesthesia on the structure of functional clusters, contributing for understanding some new aspects of neural correlates of consciousness.Comment: 24 pages, 8 figures. arXiv admin note: text overlap with arXiv:1604.0000