Efficient Coding in the Economics of Human Brain Connectomics
Dale Zhou, Christopher W. Lynn, Zaixu Cui, Rastko Ciric, Graham L. Baum, Tyler M. Moore, David R. Roalf, John A. Detre, Ruben C. Gur, Raquel E. Gur, Theodore D.… 展开作者
Dale Zhou, Christopher W. Lynn, Zaixu Cui, Rastko Ciric, Graham L. Baum, Tyler M. Moore, David R. Roalf, John A. Detre, Ruben C. Gur, Raquel E. Gur, Theodore D. Satterthwaite, Danielle S. Bassett
In systems neuroscience, most models posit that brain regions communicate information under constraints of efficiency. Yet, evidence for efficient communication in structural brain networks characterized by hierarchical organization and highly connected hubs remains sparse. The principle of efficient coding proposes that the brain transmits maximal information in a metabolically economical or compressed form to improve future behavior. To determine how structural connectivity supports efficient coding, we develop a theory specifying minimum rates of message transmission between brain regions to achieve an expected fidelity, and we test five predictions from the theory based on random walk communication dynamics. In doing so, we introduce the metric of compression efficiency, which quantifies the trade-off between lossy compression and transmission fidelity in structural networks. In a large sample of youth (n = 1,042; age 8-23 years), we analyze structural networks derived from diffusion weighted imaging and metabolic expenditure operationalized using cerebral blood flow. We show that structural networks strike compression efficiency trade-offs consistent with theoretical predictions. We find that compression efficiency prioritizes fidelity with development, heightens when metabolic resources and myelination guide communication, explains advantages of hierarchical organization, links higher input fidelity to disproportionate areal expansion, and shows that hubs integrate information by lossy compression. Lastly, compression efficiency is predictive of behavior--beyond a conventional metric--for cognitive domains including executive function, memory, complex reasoning, and social cognition. Our findings elucidate how macroscale connectivity supports efficient coding, and serve to foreground communication processes that utilize random walk dynamics constrained by network connectivity.
We propose a neural connectomics strategy called Fluorescent In-Situ Sequencing of Barcoded Individual Neuronal Connections (FISSEQ-BOINC), leveraging fluorescent in situ nucleic acid sequencing in fixed tissue (FISSEQ). FISSEQ-BOINC exhibits different properties from BOINC, which relies on bulk nucleic acid sequencing. FISSEQ-BOINC could become a scalable approach for mapping whole-mammalian-brain connectomes with rich molecular annotations.
Connectomics and network neuroscience offer quantitative scientific frameworks for modeling and analyzing networks of structurally and functionally interacting neurons, neuronal populations, and macroscopic brain areas. This shift in perspective and emphasis on distributed brain function has provided fundamental insight into the role played by the brain's network architecture in cognition, disease, development, and aging. In this chapter, we review the core concepts of human connectomics at the macroscale. From the construction of networks using functional and diffusion MRI data, to their subs…
The human braingraph, or connectome is a description of the connections of the brain: the nodes of the graph correspond to small areas of the gray matter, and two nodes are connected by an edge if a diffusion MRI-based workflow finds fibers between those brain areas. We have constructed 1015-vertex graphs from the diffusion MRI brain images of 395 human subjects and compared the individual graphs with respect to several different areas of the brain. The inter-individual variability of the graphs within different brain regions was discovered and described. We have found that the frontal and the…
At the group-level, deep brain stimulation leads to significant therapeutic benefit in a multitude of neurological and neuropsychiatric disorders. At the single-patient level, however, symptoms may sometimes persist despite "optimal" electrode placement at established treatment coordinates. This may be partly explained by limitations of disease-centric strategies that are unable to account for heterogeneous phenotypes and comorbidities observed in clinical practice. Instead, tailoring electrode placement and programming to individual patients' symptom profiles may increase the fraction of top …
The diffused nature of mild traumatic brain injury (mTBI) impacts brain white-matter pathways with potentially long-term consequences, even after initial symptoms have resolved. To understand post-mTBI recovery in adolescents, longitudinal studies are needed to determine the interplay between highly individualised recovery trajectories and ongoing development. To capture the distributed nature of mTBI and recovery, we employ connectomes to probe the brain's structural organisation. We present a diffusion MRI study on adolescent mTBI subjects scanned one day, two weeks and one year after injury…
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…
Representation of brain network interactions is fundamental to the translation of neural structure to brain function. As such, methodologies for mapping neural interactions into structural models, i.e., inference of functional connectome from neural recordings, are key for the study of brain networks. While multiple approaches have been proposed for functional connectomics based on statistical associations between neural activity, association does not necessarily incorporate causation. Additional approaches have been proposed to incorporate aspects of causality to turn functional connectomes i…
Flatiron Institute（熨斗研究所）；Harvard University（哈佛大学）；Birla Institute of Technology and Science-Pilani（比尔拉科学技术学院-皮拉尼）；Lomonosov Moscow State University（莫斯科国立罗蒙诺索夫大学）；Boston College（波士顿学院）
The size of image stacks in connectomics studies now reaches the terabyte and often petabyte scales with a great diversity of appearance across brain regions and samples. However, manual annotation of neural structures, e.g., synapses, is time-consuming, which leads to limited training data often smaller than 0.001\% of the test data in size. Domain adaptation and generalization approaches were proposed to address similar issues for natural images, which were less evaluated on connectomics data due to a lack of out-of-domain benchmarks.
Massachusetts General Hospital（麻省总医院）；Harvard Medical School（哈佛医学院）；German Center for Neurodegenerative Diseases（德国神经退行性疾病中心）；University Hospital Bonn（波恩大学医院）；Johns Hopkins University（约翰斯·霍普金斯大学）；Istanbul Technical University（伊斯坦布尔理工大学）；University of Dundee（邓迪大学）；University of North Carolina at Greensboro（北卡罗来纳大学格林斯伯勒分校）；Kennedy Krieger Institute（肯尼迪·克里格研究所）；Johns Hopkins School of Medicine（约翰斯·霍普金斯医学院）
Large, open-source consortium datasets have spurred the development of new and increasingly powerful machine learning approaches in brain connectomics. However, one key question remains: are we capturing biologically relevant and generalizable information about the brain, or are we simply overfitting to the data? To answer this, we organized a scientific challenge, the Connectomics in NeuroImaging Transfer Learning Challenge (CNI-TLC), held in conjunction with MICCAI 2019. CNI-TLC included two classification tasks: (1) diagnosis of Attention-Deficit/Hyperactivity Disorder (ADHD) within a pre-a…
Modern neuroimaging technologies, combined with state-of-the-art data processing pipelines, have made it possible to collect longitudinal observations of an individual's brain connectome at different ages. It is of substantial scientific interest to study how brain connectivity varies over time in relation to human cognitive traits. In brain connectomics, the structural brain network for an individual corresponds to a set of interconnections among brain regions. We propose a symmetric bilinear logistic regression to learn a set of small subgraphs relevant to a binary outcome from longitudinal …
Understanding brain connectivity in a network-theoretic context has shown much promise in recent years. This type of analysis identifies brain organisational principles, bringing a new perspective to neuroscience. At the same time, large public databases of connectomic data are now available. However, connectome analysis is still an emerging field and there is a crucial need for robust computational methods to fully unravelits potential. This workshop provides a platform to discuss the development of new analytic techniques; methods for evaluating and validating commonly used approaches; as we…
The human brain is the most complex object of study we encounter today. Mapping the neuronal-level connections between the more than 80 billion neurons in the brain is a hopeless task for science. By the recent advancement of magnetic resonance imaging (MRI), we are able to map the macroscopic connections between about 1000 brain areas. The MRI data acquisition and the subsequent algorithmic workflow contain several complex steps, where errors can occur. In the present contribution, we describe and publish 1064 human connectomes, computed from the public release of the Human Connectome Project…
Neuropsychiatric disorders impact functional connectivity of the brain at the network level. The identification and statistical testing of disorder-related networks remains challenging. We propose novel methods to streamline the detection and testing of the hidden, disorder-related connectivity patterns as network-objects. We define an abnormal connectome subnetwork as a network-object that includes three classes: nodes of brain areas, edges representing brain connectomic features, and an organized graph topology formed by these nodes and edges. Comparing to the conventional statistical method…
As the field of connectomics has matured, it has expanded from mapping the existence of connections between brain components to measuring the strength of connections. This information is increasingly accessible via methodologies such as pairing functional magnetic resonance (MR) imaging and MR tractography in the same human subject, as well as novel methods in non-human animals using optogenetics. Systems and network neuroscience have in recent years focused extensively on explaining correlation patterns of functional activity in the brain in terms of the degree of connectedness of brain compo…
In structural brain networks the connections of interest consist of white-matter fibre bundles between spatially segregated brain regions. The presence, location and orientation of these white matter tracts can be derived using diffusion MRI in combination with probabilistic tractography. Unfortunately, as of yet no approaches have been suggested that provide an undisputed way of inferring brain networks from tractography. In this paper, we provide a computational framework which we refer to as Bayesian connectomics. Rather than applying an arbitrary threshold to obtain a single network, we co…
It is nearly 20 years since the concept of a small-world network was first quantitatively defined, by a combination of high clustering and short path length; and about 10 years since this metric of complex network topology began to be widely applied to analysis of neuroimaging and other neuroscience data as part of the rapid growth of the new field of connectomics. Here we review briefly the foundational concepts of graph theoretical estimation and generation of small-world networks. We take stock of some of the key developments in the field in the past decade and we consider in some detail th…
The human connectome has become the very frequent subject of study of brain-scientists, psychologists, and imaging experts in the last decade. With diffusion magnetic resonance imaging techniques, unified with advanced data processing algorithms, today we are able to compute braingraphs with several hundred, anatomically identified nodes and thousands of edges, corresponding to the anatomical connections of the brain. The analysis of these graphs without refined mathematical tools is hopeless. These tools need to address the high error rate of the MRI processing workflow, and need to find stru…
Connectomics has focused primarily on the mapping of synaptic links in the brain; yet it is well established that extrasynaptic volume transmission, especially via monoamines and neuropeptides, is also critical to brain function. Here we present a draft monoamine connectome, along with a partial neuropeptide connectome, for the nematode C. elegans, based on new and published expression data for biosynthetic genes and receptors. Thus, the neuronal connectome can be represented as a multiplex network, with synaptic, gap junction, and neuromodulatory layers representing alternative modes of inter…
Recently, there have been several concerted international efforts - the BRAIN initiative, European Human Brain Project and the Human Connectome Project, to name a few - that hope to revolutionize our understanding of the connected brain. Over the past two decades, functional neuroimaging has emerged as the predominant technique in systems neuroscience. This is foreshadowed by an ever increasing number of publications on functional connectivity, causal modeling, connectomics, and multivariate analyses of distributed patterns of brain responses. In this article, we summarize pedagogically the (d…
At the inception of human brain mapping, two principles of functional anatomy underwrote most conceptions - and analyses - of distributed brain responses: namely functional segregation and integration. There are currently two main approaches to characterising functional integration. The first is a mechanistic modelling of connectomics in terms of directed effective connectivity that mediates neuronal message passing and dynamics on neuronal circuits. The second phenomenological approach usually characterises undirected functional connectivity (i.e., measurable correlations), in terms of intrin…
Investigations of the human connectome have elucidated core features of adult structural networks, particularly the crucial role of hub-regions. However, little is known regarding network organisation of the healthy elderly connectome, a crucial prelude to the systematic study of neurodegenerative disorders. Here, whole-brain probabilistic tractography was performed on high-angular diffusion-weighted images acquired from 115 healthy elderly subjects, whom were 76 to 94 years old. Structural networks were reconstructed between 512 cortical and subcortical brain regions. We sought to investigate…
The impact of developmental and aging processes on brain connectivity and the connectome has been widely studied. Network theoretical measures and certain topological principles are computed from the entire brain, however there is a need to separate and understand the underlying subnetworks which contribute towards these observed holistic connectomic alterations. One organizational principle is the rich-club - a core subnetwork of brain regions that are strongly connected, forming a high-cost, high-capacity backbone that is critical for effective communication in the network. Investigations pr…
University of Utah（犹他大学）；Florida State University（佛罗里达州立大学）；University of Vienna（维也纳大学）；University of Virginia（弗吉尼亚大学）
The goal of diffusion-weighted magnetic resonance imaging (DWI) is to infer the structural connectivity of an individual subject's brain in vivo. To statistically study the variability and differences between normal and abnormal brain connectomes, a mathematical model of the neural connections is required. In this paper, we represent the brain connectome as a Riemannian manifold, which allows us to model neural connections as geodesics. This leads to the challenging problem of estimating a Riemannian metric that is compatible with the DWI data, i.e., a metric such that the geodesic curves repr…
Istanbul Technical University（伊斯坦布尔理工大学）；University of Dundee（邓迪大学）
-Background. Network neuroscience examines the brain as a complex system represented by a network (or connectome), providing deeper insights into the brain morphology and function, allowing the identification of atypical brain connectivity alterations, which can be used as diagnostic markers of neurological disorders. -Existing Methods. Graph embedding methods which map data samples (e.g., brain networks) into a low dimensional space have been widely used to explore the relationship between samples for classification or prediction tasks. However, the majority of these works are based on modeli…
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, impl…
University of Illinois Chicago（伊利诺伊大学芝加哥分校）；University of Pittsburgh（匹兹堡大学）
Graph theoretical analyses have become standard tools in modeling functional and anatomical connectivity in the brain. With the advent of connectomics, the primary graphs or networks of interest are structural connectome (derived from DTI tractography) and functional connectome (derived from resting-state fMRI). However, most published connectome studies have focused on either structural or functional connectome, yet complementary information between them, when available in the same dataset, can be jointly leveraged to improve our understanding of the brain. To this end, we propose a function-…
For constructing neuronal network models computational neuroscientists have access to wide-ranging anatomical data that nevertheless tend to cover only a fraction of the parameters to be determined. Finding and interpreting the most relevant data, estimating missing values, and combining the data and estimates from various sources into a coherent whole is a daunting task. With this chapter we aim to provide guidance to modelers by describing the main types of anatomical data that may be useful for informing neuronal network models. We further discuss aspects of the underlying experimental tech…
Brain network is remarkably cost-efficient while the fundamental physical and dynamical mechanisms underlying its economical optimization in network structure and activity are not clear. Here we study intricate cost-efficient interplay between structure and dynamics in biologically plausible spatial modular neuronal network models. We find that critical avalanche states from excitation-inhibition balance, under modular network topology with less wiring cost, can also achieve less costs in firing, but with strongly enhanced response sensitivity to stimuli. We derived mean-field equations that g…
Encoding brain regions and their connections as a network of nodes and edges captures many of the possible paths along which information can be transmitted as humans process and perform complex behaviors. Because cognitive processes involve large and distributed networks of brain areas, examinations of multi-node routes within larger connection patterns can offer fundamental insights into the complexities of brain function. Here, we investigate both densely connected groups of nodes that could perform local computations as well as larger patterns of interactions that would allow for parallel p…
In recent years, new and important perspectives were introduced in the field of neuroimaging with the emergence of the connectionist approach. In this new context, it is important to know not only which brain areas are activated by a particular stimulus but, mainly, how these areas are structurally and functionally connected, distributed, and organized in relation to other areas. Additionally, the arrangement of the network elements, i.e., its topology, and the dynamics they give rise to are also important. This new approach is called connectomics. It brings together a series of techniques and…
Evaluating the effects of high-throughput structural neuroimaging predictors on whole-brain functional connectome outcomes via network-based vector-on-matrix regression
Mapping the connectivity of neurons in the brain (i.e., connectomics) is a challenging problem due to both the number of connections in even the smallest organisms and the nanometer resolution required to resolve them. Because of this, previous connectomes contain only hundreds of neurons, such as in the C.elegans connectome. Recent technological advances will unlock the mysteries of increasingly large connectomes (or partial connectomes). However, the value of these maps is limited by our ability to reason with this data and understand any underlying motifs. To aid connectome analysis, we int…
Network analyses in nervous system disorders involves constructing and analyzing anatomical and functional brain networks from neuroimaging data to describe and predict the clinical syndromes that result from neuropathology. A network view of neurological disease and clinical syndromes facilitates accurate quantitative characterizations and mathematical models of complex nervous system disorders with relatively simple tools drawn from the field of graph theory. Networks are predominantly constructed from in vivo data acquired using physiological and neuroimaging techniques at the macroscale of…
Istanbul Technical University（伊斯坦布尔技术大学）；University of Sousse（苏塞大学）；National School for Computer Science (ENSI)（国家计算机科学学校）；University of North Carolina at Chapel Hill（北卡罗来纳大学教堂山分校）；ShanghaiTech University（上海科技大学）；United Imaging Intelligence Co., Ltd.（联影智能有限公司）
Charting the baby connectome evolution trajectory during the first year after birth plays a vital role in understanding dynamic connectivity development of baby brains. Such analysis requires acquisition of longitudinal connectomic datasets. However, both neonatal and postnatal scans are rarely acquired due to various difficulties. A small body of works has focused on predicting baby brain evolution trajectory from a neonatal brain connectome derived from a single modality. Although promising, large training datasets are essential to boost model learning and to generalize to a multi-trajectory…
SurfAge-Net: A Hierarchical Surface-Based Network for Interpretable Fine-Grained Brain Age Prediction
Gansu Provincial Key Laboratory of Wearable Computing, School of Information Science and Engineering, Lanzhou University（甘肃省可穿戴计算重点实验室，信息科学与工程学院，兰州大学）；Department of Medical Imaging Center, Gansu Provincial Maternity and Child-Care Hospital（医学影像中心，甘肃省妇幼保健院）；Department of Magnetic Resonance, Lanzhou University Second Hospital（磁共振科，兰州大学第二医院）；Department of Computer Science and Technology, Harbin Institute of Technology (Shenzhen)（计算机科学与技术系，哈尔滨工业大学（深圳））；Key Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University（教育部生物医学工程重点实验室，生物医学工程学院，浙江大学）
Information flow provides a natural measure for the causal interaction between dynamical events. This study extends our previous rigorous formalism of componentwise information flow to the bulk information flow between two complex subsystems of a large-dimensional parental system, in order to investigate problems such as the effective connectivity between two brain regions, each with millions of neurons involved. Analytical formulas have been obtained in a closed form. Under a Gaussian assumption, their maximum likelihood estimators have also been obtained. These formulas have been validated u…
Center for Quantitative Biology, Academy for Advanced Interdisciplinary Studies, Peking University（北京大学前沿交叉学科研究院定量生物学中心）；School of Physics, Peking University（北京大学物理学院）；Center for Bioinformatics, National Laboratory of Protein Engineering and Plant Genetic Engineering, School of Life Sciences and Center for Quantitative Biology, Academy for Advanced Interdisciplinary Studies,Peking University（北京大学生命科学学院、前沿交叉学科研究院定量生物学中心及蛋白质工程与植物基因工程国家重点实验室生物信息中心）；CNRS, LJAD and Institute NeuroMod, Université Côte d’Azur（法国蔚蓝海岸大学神经调节研究所、LJAD及法国国家科学研究中心）
Lattices abound in nature - from the crystal structure of minerals to the honey-comb organization of ommatidia in the compound eye of insects. Such regular arrangements provide solutions for optimally dense packings, efficient resource distribution and cryptographic schemes, highlighting the importance of lattice theory in mathematics and physics, biology and economics, and computer science and coding theory. Do lattices also play a role in how the brain represents information? To answer this question, we focus on higher-dimensional stimulus domains, with particular emphasis on neural represen…
