Single spikes drive sequential propagation and routing of activity in a cortical network.
Ontology highlight
ABSTRACT:
SUBMITTER: Riquelme JL
PROVIDER: S-EPMC9925052 | biostudies-literature | 2023 Feb
REPOSITORIES: biostudies-literature
Publications
Single spikes drive sequential propagation and routing of activity in a cortical network.
Riquelme Juan Luis JL Hemberger Mike M Laurent Gilles G Gjorgjieva Julijana J
eLife 20230213
Single spikes can trigger repeatable firing sequences in cortical networks. The mechanisms that support reliable propagation of activity from such small events and their functional consequences remain unclear. By constraining a recurrent network model with experimental statistics from turtle cortex, we generate reliable and temporally precise sequences from single spike triggers. We find that rare strong connections support sequence propagation, while dense weak connections modulate propagation ...[more]
Similar Datasets
Project description:Disruptions in circadian rhythms and dopaminergic activity are involved in the pathophysiology of bipolar disorder, though their interaction remains unclear. Moreover, a lack of animal models that display spontaneous cycling between mood states has hindered our mechanistic understanding of mood switching. Here, we find that mice with a mutation in the circadian Clock gene (ClockΔ19) exhibit rapid mood-cycling, with a profound manic-like phenotype emerging during the day following a period of euthymia at night. Mood-cycling coincides with abnormal daytime spikes in ventral tegmental area (VTA) dopaminergic activity, tyrosine hydroxylase (TH) levels and dopamine synthesis. To determine the significance of daytime increases in VTA dopamine activity to manic behaviors, we developed a novel optogenetic stimulation paradigm that produces a sustained increase in dopamine neuronal activity and find that this induces a manic-like behavioral state. Time-dependent dampening of TH activity during the day reverses manic-related behaviors in ClockΔ19 mice. Finally, we show that CLOCK acts as a negative regulator of TH transcription, revealing a novel molecular mechanism underlying cyclic changes in mood-related behavior. Taken together, these studies have identified a mechanistic connection between circadian gene disruption and the precipitation of manic episodes in bipolar disorder.
| S-EPMC4492925 | biostudies-literature
Project description:Benign childhood epilepsy with centrotemporal spikes (BECTS) is associated with cognitive and language problems. According to recent studies, disruptions in brain structure and function in children with BECTS are beyond a Rolandic focus, suggesting atypical cortical development. However, previous studies utilizing surface-based metrics (e.g., cortical gyrification) and their structural covariance networks at high resolution in children with BECTS are limited. Twenty-six children with BECTS (15 males/11 females; 10.35 ± 2.91 years) and 26 demographically matched controls (15 males/11 females; 11.35 ± 2.51 years) were included in this study and subjected to high-resolution structural brain MRI scans. The gyrification index was calculated, and structural brain networks were reconstructed based on the covariance of the cortical folding. In the BECTS group, significantly increased gyrification was observed in the bilateral Sylvain fissures and the left pars triangularis, temporal, rostral middle frontal, lateral orbitofrontal, and supramarginal areas (cluster-corrected p < 0.05). Global brain network measures were not significantly different between the groups; however, the nodal alterations were most pronounced in the insular, frontal, temporal, and occipital lobes (FDR corrected, p < 0.05). In children with BECTS, brain hubs increased in number and tended to shift to sensorimotor and temporal areas. Furthermore, we observed significantly positive relationships between the gyrification index and age (vertex p < 0.001, cluster-level correction) as well as duration of epilepsy (vertex p < 0.001, cluster-level correction). Our results suggest that BECTS may be a condition that features abnormal over-folding of the Sylvian fissures and uncoordinated development of structural wiring, disrupted nodal profiles of centrality, and shifted hub distribution, which potentially represents a neuroanatomical hallmark of BECTS in the developing brain.
| S-EPMC5807981 | biostudies-literature
Project description:The mechanisms underlying an effective propagation of high intensity information over a background of irregular firing and response latency in cognitive processes remain unclear. Here we propose a SSCCPI circuit to address this issue. We hypothesize that when a high-intensity thalamic input triggers synchronous spike events (SSEs), dense spikes are scattered to many receiving neurons within a cortical column in layer IV, many sparse spike trains are propagated in parallel along minicolumns at a substantially high speed and finally integrated into an output spike train toward or in layer Va. We derive the sufficient conditions for an effective (fast, reliable, and precise) SSCCPI circuit: (i) SSEs are asynchronous (near synchronous); (ii) cortical columns prevent both repeatedly triggering SSEs and incorrectly synaptic connections between adjacent columns; and (iii) the propagator in interneurons is temporally complete fidelity and reliable. We encode the membrane potential responses to stimuli using the non-linear autoregressive integrated process derived by applying Newton's second law to stochastic resilience systems. We introduce a multithreshold decoder to correct encoding errors. Evidence supporting an effective SSCCPI circuit includes that for the condition, (i) time delay enhances SSEs, suggesting that response latency induces SSEs in high-intensity stimuli; irregular firing causes asynchronous SSEs; asynchronous SSEs relate to healthy neurons; and rigorous SSEs relate to brain disorders. For the condition (ii) neurons within a given minicolumn are stereotypically interconnected in the vertical dimension, which prevents repeated triggering SSEs and ensures signal parallel propagation; columnar segregation avoids incorrect synaptic connections between adjacent columns; and signal propagation across layers overwhelmingly prefers columnar direction. For the condition (iii), accumulating experimental evidence supports temporal transfer precision with millisecond fidelity and reliability in interneurons; homeostasis supports a stable fixed-point encoder by regulating changes to synaptic size, synaptic strength, and ion channel function in the membrane; together all-or-none modulation, active backpropagation, additive effects of graded potentials, and response variability functionally support the multithreshold decoder; our simulations demonstrate that the encoder-decoder is temporally complete fidelity and reliable in special intervals contained within the stable fixed-point range. Hence, the SSCCPI circuit provides a possible mechanism of effective signal propagation in cortical networks.
| S-EPMC6718730 | biostudies-literature
Project description:The role of dendritic spiking mechanisms in neural processing is so far poorly understood. To investigate the role of calcium spikes in the functional properties of the single neuron and recurrent networks, we investigated a three compartment neuron model of the layer 5 pyramidal neuron with calcium dynamics in the distal compartment. By performing single neuron simulations with noisy synaptic input and occasional large coincident input at either just the distal compartment or at both somatic and distal compartments, we show that the presence of calcium spikes confers a substantial advantage for coincidence detection in the former case and a lesser advantage in the latter. We further show that the experimentally observed critical frequency phenomenon, in which action potentials triggered by stimuli near the soma above a certain frequency trigger a calcium spike at distal dendrites, leading to further somatic depolarization, is not exhibited by a neuron receiving realistically noisy synaptic input, and so is unlikely to be a necessary component of coincidence detection. We next investigate the effect of calcium spikes in propagation of spiking activities in a feed-forward network (FFN) embedded in a balanced recurrent network. The excitatory neurons in the network are again connected to either just the distal, or both somatic and distal compartments. With purely distal connectivity, activity propagation is stable and distinguishable for a large range of recurrent synaptic strengths if the feed-forward connections are sufficiently strong, but propagation does not occur in the absence of calcium spikes. When connections are made to both the somatic and the distal compartments, activity propagation is achieved for neurons with active calcium dynamics at a much smaller number of neurons per pool, compared to a network of passive neurons, but quickly becomes unstable as the strength of recurrent synapses increases. Activity propagation at higher scaling factors can be stabilized by increasing network inhibition or introducing short term depression in the excitatory synapses, but the signal to noise ratio remains low. Our results demonstrate that the interaction of synchrony with dendritic spiking mechanisms can have profound consequences for the dynamics on the single neuron and network level.
| S-EPMC4957534 | biostudies-literature
Project description:OBJECTIVE:Although substantial progress has been made in mapping the connections of the brain, less is known about how this organization translates into brain function. In particular, the massive interconnectivity of the brain has made it difficult to specifically examine data transmission between two nodes of the connectome, a central component of the 'neural code.' Here, we investigated the propagation of multiple streams of asynchronous neuronal activity across an isolated in vitro 'connectome unit.' APPROACH:We used the novel technique of axon stretch growth to create a model of a long-range cortico-cortical network, a modular system consisting of paired nodes of cortical neurons connected by axon tracts. Using optical stimulation and multi-electrode array recording techniques, we explored how input patterns are represented by cortical networks, how these representations shift as they are transmitted between cortical nodes and perturbed by external conditions, and how well the downstream node distinguishes different patterns. MAIN RESULTS:Stimulus representations included direct, synaptic, and multiplexed responses that grew in complexity as the distance between the stimulation source and recorded neuron increased. These representations collapsed into patterns with lower information content at higher stimulation frequencies. With internodal activity propagation, a hierarchy of network pathways, including latent circuits, was revealed using glutamatergic blockade. As stimulus channels were added, divergent, non-linear effects were observed in local versus distant network layers. Pairwise difference analysis of neuronal responses suggested that neuronal ensembles generally outperformed individual cells in discriminating input patterns. SIGNIFICANCE:Our data illuminate the complexity of spiking activity propagation in cortical networks in vitro, which is characterized by the transformation of an input into myriad outputs over several network layers. These results provide insight into how the brain potentially processes information and generates the neural code and could guide the development of clinical therapies based on multichannel brain stimulation.
| S-EPMC5417339 | biostudies-literature
Project description:Resting-state functional connectivity is used throughout neuroscience to study brain organization and to generate biomarkers of development, disease, and cognition. The processes that give rise to correlated activity are, however, poorly understood. Here we decompose resting-state functional connectivity using a temporal unwrapping procedure to assess the contributions of moment-to-moment activity cofluctuations to the overall connectivity pattern. This approach temporally resolves functional connectivity at a timescale of single frames, which enables us to make direct comparisons of cofluctuations of network organization with fluctuations in the blood oxygen level-dependent (BOLD) time series. We show that surprisingly, only a small fraction of frames exhibiting the strongest cofluctuation amplitude are required to explain a significant fraction of variance in the overall pattern of connection weights as well as the network's modular structure. These frames coincide with frames of high BOLD activity amplitude, corresponding to activity patterns that are remarkably consistent across individuals and identify fluctuations in default mode and control network activity as the primary driver of resting-state functional connectivity. Finally, we demonstrate that cofluctuation amplitude synchronizes across subjects during movie watching and that high-amplitude frames carry detailed information about individual subjects (whereas low-amplitude frames carry little). Our approach reveals fine-scale temporal structure of resting-state functional connectivity and discloses that frame-wise contributions vary across time. These observations illuminate the relation of brain activity to functional connectivity and open a number of directions for future research.
| S-EPMC7668041 | biostudies-literature
Project description:Routing optimization is a relevant problem in many contexts. Solving directly this type of optimization problem is often computationally intractable. Recent studies suggest that one can instead turn this problem into one of solving a dynamical system of equations, which can instead be solved efficiently using numerical methods. This results in enabling the acquisition of optimal network topologies from a variety of routing problems. However, the actual extraction of the solution in terms of a final network topology relies on numerical details which can prevent an accurate investigation of their topological properties. In fact, in this context, theoretical results are fully accessible only to an expert audience and ready-to-use implementations for non-experts are rarely available or insufficiently documented. In particular, in this framework, final graph acquisition is a challenging problem in-and-of-itself. Here we introduce a method to extract network topologies from dynamical equations related to routing optimization under various parameters' settings. Our method is made of three steps: first, it extracts an optimal trajectory by solving a dynamical system, then it pre-extracts a network, and finally, it filters out potential redundancies. Remarkably, we propose a principled model to address the filtering in the last step, and give a quantitative interpretation in terms of a transport-related cost function. This principled filtering can be applied to more general problems such as network extraction from images, thus going beyond the scenarios envisioned in the first step. Overall, this novel algorithm allows practitioners to easily extract optimal network topologies by combining basic tools from numerical methods, optimization and network theory. Thus, we provide an alternative to manual graph extraction which allows a grounded extraction from a large variety of optimal topologies. The analysis of these may open up the possibility to gain new insights into the structure and function of optimal networks. We provide an open source implementation of the code online.
| S-EPMC7704656 | biostudies-literature
Project description:BackgroundPropagating waves of excitation have been observed extensively in the neocortex, during both spontaneous and sensory-evoked activity, and they play a critical role in spatially organizing information processing. However, the state-dependence of these spatiotemporal propagation patterns is largely unexplored. In this report, we use voltage-sensitive dye imaging in the rat visual cortex to study the propagation of spontaneous population activity in two discrete cortical states induced by urethane anesthesia.ResultsWhile laminar current source density patterns of spontaneous population events in these two states indicate a considerable degree of similarity in laminar networks, lateral propagation in the more active desynchronized state is approximately 20% faster than in the slower synchronized state. Furthermore, trajectories of wave propagation exhibit a strong anisotropy, but the preferred direction is different depending on cortical state.ConclusionsOur results show that horizontal wave propagation of spontaneous neural activity is largely dependent on the global activity states of local cortical circuits.
| S-EPMC3733618 | biostudies-literature
Project description:The wiring of the brain is organized around a putative unimodal-transmodal hierarchy. Here we investigate how this intrinsic hierarchical organization of the brain shapes the transmission of information among regions. The hierarchical positioning of individual regions was quantified by applying diffusion map embedding to resting-state functional MRI networks. Structural networks were reconstructed from diffusion spectrum imaging and topological shortest paths among all brain regions were computed. Sequences of nodes encountered along a path were then labeled by their hierarchical position, tracing out path motifs. We find that the cortical hierarchy guides communication in the network. Specifically, nodes are more likely to forward signals to nodes closer in the hierarchy and cover a range of unimodal and transmodal regions, potentially enriching or diversifying signals en route. We also find evidence of systematic detours, particularly in attention networks, where communication is rerouted. Altogether, the present work highlights how the cortical hierarchy shapes signal exchange and imparts behaviorally relevant communication patterns in brain networks.
| S-EPMC7657265 | biostudies-literature
Project description:Elongated plasmonic nanoparticles have been extensively explored over the past two decades. However, in comparison with the dipolar plasmon mode that has attracted the most interest, much less attention has been paid to multipolar plasmon modes because they are usually thought to be "dark modes", which are unable to interact with far-field light efficiently. Herein, we report on an intriguing far-field scattering phenomenon, colour routing, based on longitudinal multipolar plasmon modes supported by high-aspect-ratio single Ag nanorods. Taking advantage of the distinct far-field behaviours of the odd and even multipolar plasmon modes, we demonstrate two types of colour routing, where the incident white light can be scattered into several beams with different colours as well as different propagation directions. Because of the narrow linewidths of the longitudinal multipolar plasmon modes, there is little spectral overlap between the adjacent peaks, giving rise to outstanding colour selectivity. Our experimental results and theoretical model provide a simple yet effective picture for understanding the far-field behaviour of the longitudinal multipolar plasmon modes and the resultant colour routing phenomenon. Moreover, the outstanding colour routing capability of the high-aspect-ratio Ag nanorods enables nanoscale optical components with simple geometries for controlling the propagation of light below the diffraction limit of light.
| S-EPMC6467987 | biostudies-literature