Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks

Hormuzdi, Sheriar G.; Филиппов, М. А.; Mitropoulou, Georgia; Monyer, Hannah; Bruzzone, Roberto

doi:10.1016/j.bbamem.2003.10.023

Cited by 278 publications

(199 citation statements)

References 337 publications

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“…Because of the voltage dependency of the chemical transmission, the net outcome in the receiving DAergic neuron is tuned by its membrane potential value. A coexistence of chemical and electrical transmissions has been described in GABAergic interneuron networks (22,(46)(47)(48), and promotes highly precise synchronization of spiking activity. However, tonic spontaneous activity recorded in DAergic neuron pairs is not synchronized in vitro (11), which may be essential for a homogenous low-level DA release in the striatum in the absence of relevant stimuli.…”

Section: Chemical Transmission Relies On An Inhibition Of Ih Partiallmentioning

confidence: 99%

Chemical transmission between dopaminergic neuron pairs

Vandecasteele

Głowiński

Deniau

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Midbrain dopaminergic (DAergic) neurons play a major regulatory role in in goal-directed behavior and reinforcement learning. DAergic neuron activity, and therefore spatiotemporal properties of dopamine release, precisely encodes reward signals. Neuronal activity is shaped both by external afferences and local interactions (chemical and electrical transmissions). Numerous hints suggest the existence of chemical interactions between DAergic neurons, but direct evidence and characterization are still lacking. Here, we show, using dual patch-clamp recordings in rat brain slices, a widespread bidirectional chemical transmission between DAergic neuron pairs. Hyperpolarizing postsynaptic potentials were partially mediated by D2-like receptors, and entirely resulted from the inhibition of the hyperpolarization-activated depolarizing current (Ih). These results constitute the first evidence in paired recordings of a chemical transmission relying on conductance decrease in mammals. In addition, we show that chemical transmission and electrical synapses frequently coexist within the same neuron pair and dynamically interact to shape DAergic neuron activity.electrical synapses ͉ paired recordings ͉ substantia nigra pars compacta ͉ Ih T he substantia nigra pars compacta (SNc) is the main modulatory nucleus of basal ganglia, a network of subcortical nuclei involved in procedural learning and habit formation (1, 2). Dopaminergic (DAergic) neurons composing SNc mainly project to the dorsal striatum, the major input nucleus of basal ganglia. In striatum, dopamine (DA) potently modulates the processing of corticostriatal information (3-5), contributing to the formation of sensory-motor linkages allowing selection of adapted motor behavior in response to environmental cues.Nigrostriatal DAergic neurons display two modes of discharge: a tonic firing associated with a low but constant DA release supporting a permanent tune-up of the striatal network, and a phasic firing leading to peaks of DA release, coding for a predictive reward value and attention to salient environmental events (6-9). These modes of activity are controlled by intrinsic electrophysiological properties, external inputs, and local interactions (chemical and electrical synapses) between DAergic neurons. SNc DAergic neurons are connected by gap junctions (10), and display electrical coupling able to control their spontaneous tonic activity (11). Yet, electrical coupling might not be their sole mode of communication. Numerous hints strongly support the existence of chemical transmission. DAergic neurons are known to release DA from dendrites (12), bear autoreceptors, and display a characteristic hyperpolarization in response to DA (13,14) or DA agonist application (15, 16), and to electrical stimulation of the SNc (17) or the subthalamus (18). Moreover, ultrastructural studies revealed the presence of dendrodendritic synaptic contacts between DAergic cells in the SNc (19,20). However, a direct demonstration of neuron-to-neuron communication allowing the characteriza...

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Section: Chemical Transmission Relies On An Inhibition Of Ih Partiallmentioning

confidence: 99%

Chemical transmission between dopaminergic neuron pairs

Vandecasteele

Głowiński

Deniau

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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“…The synaptic delay for a chemical synapse is typically in the range 1-100 ms, while the synaptic delay for an electrical synapse may be only about 0.2 ms. There is now little doubt that gap junctions play a substantial role in the generation of neural rhythms [28,5], both functional [25,1,28,5] and pathological [17,51]. One natural question therefore is how does the presence of gap junction coupling affect synchronous neuronal firing [40,24,4].…”

Section: Introductionmentioning

confidence: 99%

Gap Junctions and Emergent Rhythms

Coombes

Zachariou²

2009

Coherent Behavior in Neuronal Networks

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Gap junction coupling is ubiquitous in the brain, particularly between the dendritic trees of inhibitory interneurons. Such direct non-synaptic interaction allows for direct electrical communication between cells. Unlike spike-time driven synaptic neural network models, which are event based, any model with gap junctions must necessarily involve a single neuron model that can represent the shape of an action potential. Indeed, not only do neurons communicating via gaps feel super-threshold spikes, but they also experience, and respond to, sub-threshold voltage signals. In this chapter we show that the so-called absolute integrate-and-fire model is ideally suited to such studies. At the single neuron level voltage traces for the model may be obtained in closed form, and are shown to mimic those of fastspiking inhibitory neurons. Interestingly in the presence of a slow spike adaptation current the model is shown to support periodic bursting oscillations. For both tonic and bursting modes the phase response curve can be calculated in closed form. At the network level we focus on global gap junction coupling and show how to analyze the asynchronous firing state in large networks. Importantly, we are able to determine the emergence of non-trivial network rhythms due to strong coupling instabilities. To illustrate the use of our theoretical techniques (particularly the phase-density formalism used to determine stability) we focus on a spike adaptation induced transition from asynchronous tonic activity to synchronous bursting in a gap-junction coupled network.

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“…Separate regulation of electrical and chemical synapses creates multifunctionality in neural circuits, as illustrated in the vertebrate retina, where regulation of electrical synapses rewires information flow at different light levels (1,2). Electrical synapses also have essential roles in the developing brain, where they regulate the formation of chemical synapses (3)(4)(5). In humans, mutations that affect electrical synapses are associated with neurological conditions such as epilepsy, deafness, and peripheral neuropathies (6)(7)(8).…”

mentioning

confidence: 99%

Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans

Jang

Levy

Flavell

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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A hub-and-spoke circuit of neurons connected by gap junctions controls aggregation behavior and related behavioral responses to oxygen, pheromones, and food in Caenorhabditis elegans. The molecular composition of the gap junctions connecting RMG hub neurons with sensory spoke neurons is unknown. We show here that the innexin gene unc-9 is required in RMG hub neurons to drive aggregation and related behaviors, indicating that UNC-9-containing gap junctions mediate RMG signaling. To dissect the circuit in detail, we developed methods to inhibit unc-9-based gap junctions with dominant-negative unc-1 transgenes. unc-1(dn) alters a stomatin-like protein that regulates unc-9 electrical signaling; its disruptive effects can be rescued by a constitutively active UNC-9::GFP protein, demonstrating specificity. Expression of unc-1(dn) in RMG hub neurons, ADL or ASK pheromone-sensing neurons, or URX oxygen-sensing neurons disrupts specific elements of aggregation-related behaviors. In ADL, unc-1(dn) has effects opposite to those of tetanus toxin light chain, separating the roles of ADL electrical and chemical synapses. These results reveal roles of gap junctions in a complex behavior at cellular resolution and provide a tool for similar exploration of other gap junction circuits.innexin | neural circuits | electrical synapses | stomatin | sensory behavior

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Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks

Cited by 278 publications

References 337 publications

Chemical transmission between dopaminergic neuron pairs

Chemical transmission between dopaminergic neuron pairs

Gap Junctions and Emergent Rhythms

Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans

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