Cognitive function requires the coordination of neural activity across many scales, from neurons and circuits to large-scale networks. As such, it is unlikely that an explanatory framework focused upon any single scale will yield a comprehensive theory of brain activity and cognitive function. Modelling and analysis methods for neuroscience should aim to accommodate multiscale phenomena. Emerging research now suggests that multi-scale processes in the brain arise from so-called critical phenomena that occur very broadly in the natural world. Criticality arises in complex systems perched between order and disorder, and is marked by fluctuations that do not have any privileged spatial or temporal scale. We review the core nature of criticality, the evidence supporting its role in neural systems and its explanatory potential in brain health and disease.Keywords: Bifurcations; metastability; multistability; dynamics; power-law; cognition. Highlights Criticality is a wide-spread phenomenon in natural systems Criticality provides a unifying framework to model and understand brain activity and cognitive function Substantial evidence now supports the hypothesis that the brain operates near criticality We review the role of criticality in healthy and pathological brain dynamics Caveats and pitfalls regarding the assessment of criticality in the brain are discussed *
Brain structure reflects the influence of evolutionary processes that pit the costs of its anatomical wiring against the computational advantages conferred by its complexity. We show that cost-neutral 'mutations' of the human connectome almost inevitably degrade its complexity and disconnect high-strength connections to prefrontal network hubs. Conversely, restoring the peripheral location and strong connectivity of empirically observed hubs confers a wiring cost that the brain appears to minimize. Progressive cost-neutral randomization yields daughter networks that differ substantially from one another and results in a topologically unstable phenomenon consistent with a phase transition in complex systems. The fragility of hubs to disconnection shows a significant association with the acceleration of gray matter loss in schizophrenia. Together with effects on wiring cost, we suggest that fragile prefrontal hub connections and topological volatility act as evolutionary influences on brain networks whose optimal set point may be perturbed in neuropsychiatric disorders.
Traveling patterns of neuronal activity -brain waves -have been observed across a breadth of neuronal recordings, states of awareness, and species, but their emergence in the human brain lacks a firm understanding. Here, we analyze the complex nonlinear dynamics that emerge from modeling large-scale spontaneous neural activity on a whole-brain network derived from human tractography. We find a rich array of three-dimensional wave patterns, including traveling waves, spiral waves, sources, and sinks. These patterns are metastable, such that multiple spatiotemporal wave patterns are visited in sequence. Transitions between states correspond to reconfigurations of underlying phase flows, characterized by nonlinear instabilities. These metastable dynamics accord with empirical data from multiple imaging modalities, including electrical waves in cortical tissue, sequential spatiotemporal patterns in resting-state MEG data, and large-scale waves in human electrocorticography. By moving the study of functional networks from a spatially static to an inherently dynamic (wave-like) frame, our work unifies apparently diverse phenomena across functional neuroimaging modalities and makes specific predictions for further experimentation.
Rapid reconfigurations of brain activity support efficient neuronal communication and flexible behaviour. Suboptimal brain dynamics is associated to impaired adaptability, possibly leading to functional deficiencies. We hypothesize that impaired flexibility in brain activity can lead to motor and cognitive symptoms of Parkinson’s disease (PD). To test this hypothesis, we studied the ‘functional repertoire’—the number of distinct configurations of neural activity—using source-reconstructed magnetoencephalography in PD patients and controls. We found stereotyped brain dynamics and reduced flexibility in PD. The intensity of this reduction was proportional to symptoms severity, which can be explained by beta-band hyper-synchronization. Moreover, the basal ganglia were prominently involved in the abnormal patterns of brain activity. Our findings support the hypotheses that: symptoms in PD relate to impaired brain flexibility, this impairment preferentially involves the basal ganglia, and beta-band hypersynchronization is associated with reduced brain flexibility. These findings highlight the importance of extensive functional repertoires for correct behaviour.
Directionality is a fundamental feature of network connections. Most structural brain networks are intrinsically directed because of the nature of chemical synapses, which comprise most neuronal connections. Because of the limitations of noninvasive imaging techniques, the directionality of connections between structurally connected regions of the human brain cannot be confirmed. Hence, connections are represented as undirected, and it is still unknown how this lack of directionality affects brain network topology. Using six directed brain networks from different species and parcellations (cat, mouse, C. elegans, and three macaque networks), we estimate the inaccuracies in network measures (degree, betweenness, clustering coefficient, path length, global efficiency, participation index, and small-worldness) associated with the removal of the directionality of connections. We employ three different methods to render directed brain networks undirected: (a) remove unidirectional connections, (b) add reciprocal connections, and (c) combine equal numbers of removed and added unidirectional connections. We quantify the extent of inaccuracy in network measures introduced through neglecting connection directionality for individual nodes and across the network. We find that the coarse division between core and peripheral nodes remains accurate for undirected networks. However, hub nodes differ considerably when directionality is neglected. Comparing the different methods to generate undirected networks from directed ones, we generally find that the addition of reciprocal connections (false positives) causes larger errors in graph-theoretic measures than the removal of the same number of directed connections (false negatives). These findings suggest that directionality plays an essential role in shaping brain networks and highlight some limitations of undirected connectomes.
Background and Objectives:Amyotrophic lateral sclerosis (ALS) is a multisystem disorder, as supported by clinical, molecular and neuroimaging evidence. As a consequence, predicting clinical features requires a description of large-scale neuronal dynamics. Normally, brain activity dynamically reconfigures over time, recruiting different brain areas. Brain pathologies induce stereotyped dynamics which, in turn, are linked to clinical impairment. Hence, based on recent evidence showing that brain functional networks become hyper-connected as ALS progresses, we hypothesized that the loss of flexible dynamics in ALS would predict the symptoms severity.Methods:To test this hypothesis, we quantified flexibility utilizing the “functional repertoire” (i.e. the number of configurations of active brain areas) as measured from source-reconstructed magnetoencephalography (MEG) in ALS patients and healthy controls. The activity of brain areas was reconstructed in the classical frequency bands, and the functional repertoire was estimated to quantify spatio-temporal fluctuations of brain activity. Finally, we built a k-fold cross validated multilinear model to predict the individual clinical impairment from the size of the functional repertoire.Results:Comparing 42 ALS patients and 42 healthy controls, we found a more stereotyped brain dynamics in ALS patients (P < 0.05), as conveyed by the smaller functional repertoire. The relationship between the size of the functional repertoire and the clinical scores in the ALS group showed significant correlations in both the delta and the theta frequency bands. Furthermore, through a k-fold cross validated multilinear regression model, we found that the functional repertoire predicted both clinical staging (P < 0.001 and P < 0.01, in delta and theta bands, respectively) and symptoms severity (P < 0.001, in both delta and theta bands).Discussion:Our work shows that: 1) ALS pathology reduces the flexibility of large-scale brain dynamics; 2) sub-cortical regions play a key role in determining brain dynamics; 3) reduced brain flexibility predicts disease stage as well as symptoms severity. Our approach provides a non-invasive tool to quantify alterations in brain dynamics in ALS (and, possibly, other neurodegenerative diseases), thus opening new opportunities in disease management as well as a framework to test, in the near future, the effects of disease-modifying interventions at the whole-brain level.
Table of contentsA1 Functional advantages of cell-type heterogeneity in neural circuitsTatyana O. SharpeeA2 Mesoscopic modeling of propagating waves in visual cortexAlain DestexheA3 Dynamics and biomarkers of mental disordersMitsuo KawatoF1 Precise recruitment of spiking output at theta frequencies requires dendritic h-channels in multi-compartment models of oriens-lacunosum/moleculare hippocampal interneuronsVladislav Sekulić, Frances K. SkinnerF2 Kernel methods in reconstruction of current sources from extracellular potentials for single cells and the whole brainsDaniel K. Wójcik, Chaitanya Chintaluri, Dorottya Cserpán, Zoltán SomogyváriF3 The synchronized periods depend on intracellular transcriptional repression mechanisms in circadian clocks.Jae Kyoung Kim, Zachary P. Kilpatrick, Matthew R. Bennett, Kresimir JosićO1 Assessing irregularity and coordination of spiking-bursting rhythms in central pattern generatorsIrene Elices, David Arroyo, Rafael Levi, Francisco B. Rodriguez, Pablo VaronaO2 Regulation of top-down processing by cortically-projecting parvalbumin positive neurons in basal forebrainEunjin Hwang, Bowon Kim, Hio-Been Han, Tae Kim, James T. McKenna, Ritchie E. Brown, Robert W. McCarley, Jee Hyun ChoiO3 Modeling auditory stream segregation, build-up and bistabilityJames Rankin, Pamela Osborn Popp, John RinzelO4 Strong competition between tonotopic neural ensembles explains pitch-related dynamics of auditory cortex evoked fieldsAlejandro Tabas, André Rupp, Emili Balaguer-BallesterO5 A simple model of retinal response to multi-electrode stimulationMatias I. Maturana, David B. Grayden, Shaun L. Cloherty, Tatiana Kameneva, Michael R. Ibbotson, Hamish MeffinO6 Noise correlations in V4 area correlate with behavioral performance in visual discrimination taskVeronika Koren, Timm Lochmann, Valentin Dragoi, Klaus ObermayerO7 Input-location dependent gain modulation in cerebellar nucleus neuronsMaria Psarrou, Maria Schilstra, Neil Davey, Benjamin Torben-Nielsen, Volker SteuberO8 Analytic solution of cable energy function for cortical axons and dendritesHuiwen Ju, Jiao Yu, Michael L. Hines, Liang Chen, Yuguo YuO9 C. elegans interactome: interactive visualization of Caenorhabditis elegans worm neuronal networkJimin Kim, Will Leahy, Eli ShlizermanO10 Is the model any good? Objective criteria for computational neuroscience model selectionJustas Birgiolas, Richard C. Gerkin, Sharon M. CrookO11 Cooperation and competition of gamma oscillation mechanismsAtthaphon Viriyopase, Raoul-Martin Memmesheimer, Stan GielenO12 A discrete structure of the brain wavesYuri Dabaghian, Justin DeVito, Luca PerottiO13 Direction-specific silencing of the Drosophila gaze stabilization systemAnmo J. Kim, Lisa M. Fenk, Cheng Lyu, Gaby MaimonO14 What does the fruit fly think about values? A model of olfactory associative learningChang Zhao, Yves Widmer, Simon Sprecher,Walter SennO15 Effects of ionic diffusion on power spectra of local field potentials (LFP)Geir Halnes, Tuomo Mäki-Marttunen, Daniel Keller, Klas H. Pettersen,Ole A. Andreassen...
The vast tree-like dendritic structure of neurons allow them to receive and integrate input from many neurons. A wide variety of neuronal morphologies exist, however, their role in dendritic integration, and how it shapes the response of the neuron, is not yet fully understood. Here, we study the evolution and interactions of dendritic spikes in excitable neurons with complex real branch structures. We focus on dozens of digitally reconstructed illustrative neurons from the online repository NeuroMorpho.org, which contains over 100,000 neurons. Yet, our methods can be promptly extended to any other neuron. This approach allows us to estimate and map the heterogeneity of activity patterns observed across extensive dendritic trees with thousands of compartments. We propose a classification of neurons based on the location of the soma (centrality) and the dendritic topology (number of branches connected to the soma). These are key topological factors in determining the neuron's energy consumption, dynamics, and the dynamic range, which quantifies the range in synaptic input rate that can be reliably encoded by the neuron's firing rate. Moreover, we find that bifurcations, the structural building blocks of complex dendrites, play a major role in increasing the dynamic range of neurons. Our results provide a better understanding of the effects of neuronal morphology in the diversity of neuronal dynamics and function.
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