Beyond plasticity: the dynamic impact of electrical synapses on neural circuits

Abstract

Electrical synapses are found in vertebrate and invertebrate nervous systems. The cellular basis of these synapses is the gap junction, a group of intercellular channels that mediate direct communication between adjacent neurons. Similar to chemical synapses, electrical connections are modifiable and their variations in strength provide a mechanism for reconfiguring neural circuits. In addition, electrical synapses dynamically regulate neural circuits through properties without equivalence in chemical transmission. Because of their continuous nature and bidirectionality, electrical synapses allow electrical currents underlying changes in membrane potential to leak to ‘coupled’ partners, dampening neuronal excitability and altering their integrative properties. Remarkably, this effect can be transiently alleviated when comparable changes in membrane potential simultaneously occur in each of the coupled neurons, a phenomenon that is dynamically dictated by the timing of arriving signals such as synaptic potentials. By way of this mechanism, electrical synapses influence synaptic integration and action potential generation, imparting an additional layer of dynamic complexity to neural circuits.

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Fig. 1: The two main modalities of synaptic transmission and their functional characteristics.
Fig. 2: Electrical transmission and passive properties are interdependent.
Fig. 3: Electrical synapses operate at multiple strengths.
Fig. 4: The effect of electrical synapses on cell excitability is dynamic.
Fig. 5: Coincidence in electrically coupled networks modifies neuronal integration.
Fig. 6: Cellular localization of electrical synapses.

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Acknowledgements

The authors thank D. S. Faber and A. Marty for valuable comments on the manuscript. The authors are indebted to the 2013 Grass Laboratory for the stimulating environment. The authors are supported by the Grass Foundation, the Munich Center for NeuroSciences (P.A.) and US National Institutes of Health grants DC03186, DC011099, NS055726, NS085772 and NS0552827 (A.E.P.).

Reviewer information

Nature Reviews Neuroscience thanks G. Awatramani, E. Marder and M. Veruki for their contribution to the peer review of this work.

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The authors both researched data for the article, provided substantial contributions to discussion of the content, wrote the article and reviewed and edited the manuscript before submission.

Correspondence to Alberto E. Pereda.

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Glossary

Neurons of the mesencephalic nucleus of the trigeminus

Neurons of the mesencephalic nucleus of the trigeminus (MesV) are a class of primary afferents that innervate the spindles of jaw closer muscles and mechanoreceptors of periodontal ligaments. Unlike their counterparts in sensory ganglia, their large unipolar somata are located within the CNS and are distributed within the brainstem.

Cerebellar Golgi cells

Golgi cells are local inhibitory interneurons in the granule cell layer of the cerebellum. They regulate input signals to the cerebellar cortex by inhibiting granule cells.

Mauthner cells

A pair of large reticulospinal medullary neurons that mediate sensory-evoked escape responses in fish.

Amacrine type AII cells

Amacrine cells are a class of retinal interneurons. Type AII amacrine cells relay information originated in rod photoreceptors through the ON centre cone bipolar axons to ON centre ganglion cells by way of electrical synapses.

Coincidence detection

The term coincidence detection is used to describe a process by which neurons or neural circuits are capable of encoding information by detecting the occurrence of temporally close signals.

Retzius cells

Retzius cells are two large serotoninergic neurons present at each of the 21 segmental ganglia of the leech (Hirudo medicinalis) nervous system. They are involved in swimming, bending and learning behaviours.

Stomatogastric ganglion

(STG). The STG represents a group of near 30 neurons located on the stomach of decapod crustaceans, which control its rhythmic motor behaviour. These neurons are organized in two central pattern generators, pyloric and gastric, responsible for dilation and constriction of the pyloric region and chewing, respectively.

HVC nucleus

The HVC (formerly ‘high vocal centre’) is a premotor nucleus in the brain of songbirds that has a key role in song production. It contains neurons that encode timing during the song.

Law of dynamic polarization

Introduced by Ramón y Cajal, the neuron doctrine argues that the individual neuron is the unit of structure and function of the nervous system. Adding to this notion, the law of dynamic polarization postulates the presence of a unidirectional flow of information within neurons, from their dendrites (input region) and cell bodies to the axons, which constitute their output region.

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