scholarly journals Chronic electrical stimulation homeostatically decreases spontaneous activity, but paradoxically increases evoked network activity

2013 ◽  
Vol 109 (7) ◽  
pp. 1824-1836 ◽  
Author(s):  
Anubhuti Goel ◽  
Dean V. Buonomano
Keyword(s):  
Electrical Stimulation ◽  
Spontaneous Activity ◽  
External Input ◽  
Homeostatic Plasticity ◽  
Network Activity ◽  
Chronic Stimulation ◽  
Learning Rules ◽  
Chronic Electrical Stimulation ◽  
Evoked Activity

Neural dynamics generated within cortical networks play a fundamental role in brain function. However, the learning rules that allow recurrent networks to generate functional dynamic regimes, and the degree to which these regimes are themselves plastic, are not known. In this study we examined plasticity of network dynamics in cortical organotypic slices in response to chronic changes in activity. Studies have typically manipulated network activity pharmacologically; we used chronic electrical stimulation to increase activity in in vitro cortical circuits in a more physiological manner. Slices were stimulated with “implanted” electrodes for 4 days. Chronic electrical stimulation or treatment with bicuculline decreased spontaneous activity as predicted by homeostatic learning rules. Paradoxically, however, whereas bicuculline decreased evoked network activity, chronic stimulation actually increased the likelihood that evoked stimulation elicited polysynaptic activity, despite a decrease in evoked monosynaptic strength. Furthermore, there was an inverse correlation between spontaneous and evoked activity, suggesting a homeostatic tradeoff between spontaneous and evoked activity. Within-slice experiments revealed that cells close to the stimulated electrode exhibited more evoked polysynaptic activity and less spontaneous activity than cells close to a control electrode. Collectively, our results establish that chronic stimulation changes the dynamic regimes of networks. In vitro studies of homeostatic plasticity typically lack any external input, and thus neurons must rely on “spontaneous” activity to reach homeostatic “set points.” However, in the presence of external input we propose that homeostatic learning rules seem to shift networks from spontaneous to evoked regimes.

scholarly journals Homeostatic plasticity and external input shape neural network dynamics

2018 ◽  
Author(s):  
Johannes Zierenberg ◽  
Jens Wilting ◽  
Viola Priesemann
Keyword(s):  
Neural Network ◽  
Brain Area ◽  
External Input ◽  
Homeostatic Plasticity ◽  
Dynamic State ◽  
Network Topologies ◽  
Neural Network Dynamics ◽  
Spiking Activity

In vitro and in vivo spiking activity clearly differ. Whereas networks in vitro develop strong bursts separated by periods of very little spiking activity, in vivo cortical networks show continuous activity. This is puzzling considering that both networks presumably share similar single-neuron dynamics and plasticity rules. We propose that the defining difference between in vitro and in vivo dynamics is the strength of external input. In vitro, networks are virtually isolated, whereas in vivo every brain area receives continuous input. We analyze a model of spiking neurons in which the input strength, mediated by spike rate homeostasis, determines the characteristics of the dynamical state. In more detail, our analytical and numerical results on various network topologies show consistently that under increasing input, homeostatic plasticity generates distinct dynamic states, from bursting, to close-to-critical, reverberating and irregular states. This implies that the dynamic state of a neural network is not fixed but can readily adapt to the input strengths. Indeed, our results match experimental spike recordings in vitro and in vivo: the in vitro bursting behavior is consistent with a state generated by very low network input (< 0.1%), whereas in vivo activity suggests that on the order of 1% recorded spikes are input-driven, resulting in reverberating dynamics. Importantly, this predicts that one can abolish the ubiquitous bursts of in vitro preparations, and instead impose dynamics comparable to in vivo activity by exposing the system to weak long-term stimulation, thereby opening new paths to establish an in vivo-like assay in vitro for basic as well as neurological studies.

scholarly journals Oxytocin shapes spontaneous activity patterns in the developing visual cortex by activating somatostatin interneurons

2019 ◽  
Author(s):  
Paloma P Maldonado ◽  
Alvaro Nuno-Perez ◽  
Jan Kirchner ◽  
Elizabeth Hammock ◽  
Julijana Gjorgjieva ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Spontaneous Activity ◽  
Sensory Processing ◽  
Activity Patterns ◽  
Network Activity ◽  
Synaptic Connections ◽  
Pairwise Correlations ◽  
Early Brain Development

SummarySpontaneous network activity shapes emerging neuronal circuits during early brain development, however how neuromodulation influences this activity is not fully understood. Here, we report that the neuromodulator oxytocin powerfully shapes spontaneous activity patterns. In vivo, oxytocin strongly decreased the frequency and pairwise correlations of spontaneous activity events in visual cortex (V1), but not in somatosensory cortex (S1). This differential effect was a consequence of oxytocin only increasing inhibition in V1 and increasing both inhibition and excitation in S1. The increase in inhibition was mediated by the depolarization and increase in excitability of somatostatin+ (SST) interneurons specifically. Accordingly, silencing SST+ neurons pharmacogenetically fully blocked oxytocin’s effect on inhibition in vitro as well its effect on spontaneous activity patterns in vivo. Thus, oxytocin decreases the excitatory/inhibitory ratio and modulates specific features of V1 spontaneous activity patterns that are crucial for refining developing synaptic connections and sensory processing later in life.

Homeostatic Plasticity in the CNS

2019 ◽  
Author(s):  
Peter Wenner ◽  
Pernille Bülow
Keyword(s):  
Homeostatic Plasticity ◽  
Network Activity ◽  
Signaling Cascades ◽  
Neural Function ◽  
Activity Levels ◽  
Membrane Excitability ◽  
Activity Burst ◽  
Intrinsic Plasticity

Homeostatic plasticity refers to a collection of mechanisms that function to homeostatically maintain some feature of neural function. The field began with the view that homeostatic plasticity exists predominantly for the maintenance of spike rate. However, it has become clear that multiple features undergo some form of homeostatic control, including network activity, burst rate, or synaptic strength. There are several different forms of homeostatic plasticity, which are typically triggered following perturbations in activity levels. Homeostatic intrinsic plasticity (HIP) appears to compensate for the perturbation with changes in membrane excitability (voltage-gated conductances); synaptic scaling is thought to be a multiplicative increase or decrease of synaptic strengths throughout the cell following an activity perturbation; presynaptic homeostatic plasticity is a change in probability of release following a perturbation to postsynaptic receptor activity. Each form of homeostatic plasticity can be different in terms of the mechanisms that are engaged, the feature that is homeostatically regulated, the trigger that initiates the compensation, and the signaling cascades that mediate these processes. Homeostatic plasticity is often described in development, but can extend into maturity and has been described in vitro and in vivo.

scholarly journals Chronic Electrical Stimulation Promotes the Excitability and Plasticity of ESC-derived Neurons following Glutamate-induced Inhibition In vitro

2018 ◽  
Vol 8 (1) ◽  
Author(s):  
Charles-Francois V. Latchoumane ◽  
LaDonya Jackson ◽  
Mohammad S. Eslampanah Sendi ◽  
Kayvan F. Tehrani ◽  
Luke J. Mortensen ◽  
...  
Keyword(s):  
Electrical Stimulation ◽  
Chronic Electrical Stimulation

Biphasic Modulation of Spinal Visceral Nociceptive Transmission From the Rostroventral Medial Medulla in the Rat

2002 ◽  
Vol 87 (5) ◽  
pp. 2225-2236 ◽  
Author(s):  
M. Zhuo ◽  
J. N. Sengupta ◽  
G. F. Gebhart
Keyword(s):  
Electrical Stimulation ◽  
Spontaneous Activity ◽  
Low Dose ◽  
Ibotenic Acid ◽  
Spinal Neurons ◽  
Colorectal Distension ◽  
Nociceptive Transmission ◽  
Spontaneous Activities ◽  
Dependent Inhibition ◽  
Evoked Activity

Descending inhibitory and facilitatory influences from the rostroventral medulla (RVM) on responses of lumbosacral spinal neurons to noxious colorectal distension (CRD, 80 mmHg, 20 s) were studied. At 25 sites in the RVM, electrical stimulation produced biphasic effects, facilitating responses of spinal neurons to CRD at lesser intensities of stimulation (5–25 μA) and inhibiting responses of the same neurons at greater intensities of stimulation (50–100 μA). At 38 other sites in the RVM, electrical stimulation produced only intensity-dependent inhibition of neuron responses to CRD. At another 13 sites in the RVM, electrical stimulation (5–100 μA) produced only facilitatory effects on responses to CRD. Descending modulatory effects were selective for distension-evoked activity; spontaneous activities of the same spinal neurons were not significantly affected by electrical stimulation that either facilitated or inhibited neuron responses to CRD. Neuron responses to graded CRD (20–100 mmHg) were positively accelerating functions that were shifted leftward or rightward, respectively, by lesser, facilitatory intensities or greater, inhibitory intensities of RVM stimulation. l-glutamate microinjection into the RVM replicated the effects of electrical stimulation, producing similar biphasic modulatory effects as produced by electrical stimulation. Microinjection of glutamate into the RVM at a low dose (5 nmoles) facilitated responses of spinal neurons to CRD and inhibited responses of the same neurons at a greater dose (50 nmoles). In some experiments, microinjection of lidocaine (0.5 μl of 4% solution) or the neurotoxin ibotenic acid (0.5 μl, 10 μg) into the RVM produced reversible or long-lasting, respectively, decreases in spontaneous activity and responses of spinal neurons to CRD. These results reveal that spinal visceral nociceptive transmission is subject to a tonic descending excitatory influence from the RVM and that descending modulatory effects from the RVM on visceral nociceptive transmission are qualitatively similar to modulation of cutaneous nociceptive transmission.

scholarly journals A dynamic role for dopamine receptors in the control of mammalian spinal networks

2019 ◽  
Author(s):  
Simon A. Sharples ◽  
Nicole E. Burma ◽  
Joanna Borowska-Fielding ◽  
Charlie H.T. Kwok ◽  
Shane E.A. Eaton ◽  
...  
Keyword(s):  
Neural Networks ◽  
Spinal Cord ◽  
Dopamine Receptors ◽  
Spontaneous Activity ◽  
Network Activity ◽  
Network State ◽  
Endogenous Dopamine ◽  
Network Output ◽  
Spinal Network

AbstractDopamine is well known to regulate movement through the differential control of direct and indirect pathways in the striatum that express D1 and D2 receptors respectively. The spinal cord also expresses all dopamine receptors however; how the specific receptors regulate spinal network output in mammals is poorly understood. We explore the receptor-specific mechanisms that underlie dopaminergic control of spinal network output of neonatal mice during changes in spinal network excitability. During spontaneous activity, which is a characteristic of developing spinal networks operating in a low excitability state, we found that dopamine is primarily inhibitory. We uncover an excitatory D1-mediated effect of dopamine on motoneurons and network output that also involves co-activation with D2 receptors. Critically, these excitatory actions require higher concentrations of dopamine; however, analysis of dopamine concentrations of neonates indicates that endogenous levels of spinal dopamine are low. Because endogenous levels of spinal dopamine are low, this excitatory dopaminergic pathway is likely physiologically-silent at this stage in development. In contrast, the inhibitory effect of dopamine, at low physiological concentrations is mediated by parallel activation of D2, D3, D4 and α2 receptors which is reproduced when endogenous dopamine levels are increased by blocking dopamine reuptake and metabolism. We provide evidence in support of dedicated spinal network components that are controlled by excitatory D1 and inhibitory D2 receptors that is reminiscent of the classic dopaminergic indirect and direct pathway within the striatum. These results indicate that network state is an important factor that dictates receptor-specific and therefore dose-dependent control of neuromodulators on spinal network output and advances our understanding of how neuromodulators regulate neural networks under dynamically changing excitability.Significance statementMonoaminergic neuromodulation of neural networks is dependent not only on target receptors but also on network state. We studied the concentration-dependent control of spinal networks of the neonatal mouse, in vitro, during a low excitability state characterized by spontaneous network activity. Spontaneous activity is an essential element for the development of networks. Under these conditions, we defined converging receptor and cellular mechanisms that contribute to the diverse, concentration-dependent control of spinal motor networks by dopamine, in vitro. These experiments advance understanding of how monoamines modulate neuronal networks under dynamically changing excitability conditions and provide evidence of dedicated D1 and D2 regulated network components in the spinal cord that are consistent with those reported in the striatum.

scholarly journals Evaluation of in vitro neuronal networks for the study of spontaneous activity

STEMedicine ◽  
2020 ◽  
Vol 1 (2) ◽  
pp. e35 ◽  
Author(s):  
Diletta Pozzi
Keyword(s):  
Nervous System ◽  
Spontaneous Activity ◽  
Time Course ◽  
Neuronal Networks ◽  
Brain Slices ◽  
In Vitro Models ◽  
Network Activity ◽  
External Stimuli

In the absence of external stimuli, the nervous system exhibits a spontaneous electrical activity whose functions are not fully understood, and that represents the background noise of brain operations. Spontaneous activity has been proven to arise not only in vivo, but in in vitro neuronal networks as well, following some stereotypical patterns that reproduce the time course of development of the mammalian nervous system. This review provides an overview of in vitro models for the study of spontaneous network activity, discussing their ability to reproduce in vivo - like dynamics and the main findings obtained with each particular model. While explanted brain slices are able to reproduce the neuronal oscillations typically observed in anaesthetized animals, dissociated cultures allow the use of patient-derived neurons and limit the number of animals used for sample preparation.

scholarly journals Channelrhodopsin variants engage distinct patterns of network activity

2018 ◽  
Author(s):  
Na Young Jun ◽  
Jessica A. Cardin
Keyword(s):  
Network Activity ◽  
Local Network ◽  
Gamma Range ◽  
Cell Type Specific ◽  
Evoked Activity ◽  
Gamma Band Activity ◽  
Circuit Function ◽  
Temporal Profiles

AbstractChannelrhodopsins (ChRs) are light-gated ion channels that enable cell type-specific activation of neurons or neural circuits. Channelrhodopsin-2 has been widely used as a tool to probe circuit function in vitro and in vivo. Several recently developed ChR variants are characterized by faster kinetics and reduced desensitization. However, little is known about how their varying properties may regulate their interaction with local network dynamics. We compared ChR-evoked patterns of multi-unit activity and local field potentials in primary visual cortex of mice expressing three ChR variants with distinct temporal profiles: Chronos, Chrimson, and ChR2. We assessed overall activation of by measuring the amplitude and temporal progression of evoked spiking. Using gamma-range (30-80Hz) LFP power as an assay for local network engagement, we examined the recruitment of cortical network activity by each tool. All ChR variants caused light-evoked increases in firing in vivo, but each demonstrated different temporal patterning of evoked activity. In addition, the three ChRs had distinct effects on cortical gamma-band activity. Our findings suggest that variations in the kinetics of optogenetic tools can substantially affect their efficacy in neural networks in vivo, as well as the manner in which their activation engages circuit resonance.

scholarly journals Early prediction of developing spontaneous activity in cultured neuronal networks

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
David Cabrera-Garcia ◽  
Davide Warm ◽  
Pablo de la Fuente ◽  
M. Teresa Fernández-Sánchez ◽  
Antonello Novelli ◽  
...  
Keyword(s):  
Machine Learning ◽  
Spontaneous Activity ◽  
Early Development ◽  
Neuronal Network ◽  
Multivariate Adaptive Regression Splines ◽  
Network Activity ◽  
Support Vector ◽  
Neuronal Cultures ◽  
Neuronal Network Activity

AbstractSynchronization and bursting activity are intrinsic electrophysiological properties of in vivo and in vitro neural networks. During early development, cortical cultures exhibit a wide repertoire of synchronous bursting dynamics whose characterization may help to understand the parameters governing the transition from immature to mature networks. Here we used machine learning techniques to characterize and predict the developing spontaneous activity in mouse cortical neurons on microelectrode arrays (MEAs) during the first three weeks in vitro. Network activity at three stages of early development was defined by 18 electrophysiological features of spikes, bursts, synchrony, and connectivity. The variability of neuronal network activity during early development was investigated by applying k-means and self-organizing map (SOM) clustering analysis to features of bursts and synchrony. These electrophysiological features were predicted at the third week in vitro with high accuracy from those at earlier times using three machine learning models: Multivariate Adaptive Regression Splines, Support Vector Machines, and Random Forest. Our results indicate that initial patterns of electrical activity during the first week in vitro may already predetermine the final development of the neuronal network activity. The methodological approach used here may be applied to explore the biological mechanisms underlying the complex dynamics of spontaneous activity in developing neuronal cultures.

scholarly journals Degradation of Temporal Resolution in the Auditory Midbrain After Prolonged Deafness Is Reversed by Electrical Stimulation of the Cochlea

2005 ◽  
Vol 93 (6) ◽  
pp. 3339-3355 ◽  
Author(s):  
Maike Vollmer ◽  
Patricia A. Leake ◽  
Ralph E. Beitel ◽  
Stephen J. Rebscher ◽  
Russell L. Snyder
Keyword(s):  
Electrical Stimulation ◽  
Auditory System ◽  
Temporal Resolution ◽  
Central Nucleus ◽  
Central Auditory System ◽  
Auditory Midbrain ◽  
Chronic Stimulation ◽  
Spiral Ganglion Cell ◽  
Chronic Electrical Stimulation

In an animal model of prelingual deafness, we examined the anatomical and physiological effects of prolonged deafness and chronic electrical stimulation on temporal resolution in the adult central auditory system. Maximum following frequencies ( Fmax) and first spike latencies of single neurons responding to electrical pulse trains were evaluated in the inferior colliculus of two groups of neonatally deafened cats after prolonged periods of deafness (>2.5 yr): the first group was implanted with an intracochlear electrode and studied acutely (long-deafened unstimulated, LDU); the second group (LDS) received a chronic implant and several weeks of electrical stimulation (pulse rates ≥300 pps). Acutely deafened and implanted adult cats served as controls. Spiral ganglion cell density in all long-deafened animals was markedly reduced (mean <5.8% of normal). Both long-term deafness and chronic electrical stimulation altered temporal resolution of neurons in the central nucleus (ICC) but not in the external nucleus. Specifically, LDU animals exhibited significantly poorer temporal resolution of ICC neurons (lower Fmax, longer response latencies) as compared with control animals. In contrast, chronic stimulation in LDS animals led to a significant increase in temporal resolution. Changes in temporal resolution after long-term deafness and chronic stimulation occurred broadly across the entire ICC and were not correlated with its tonotopic gradient. These results indicate that chronic electrical stimulation can reverse the degradation in temporal resolution in the auditory midbrain after long-term deafness and suggest the importance of factors other than peripheral pathology on plastic changes in the temporal processing capabilities of the central auditory system.

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