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Electrical synapses between Gaba-Releasing interneurons

Nature Reviews Neuroscience volume 2, pages 425–433 (2001)Cite this article

Key Points

  • Although most synapses in the vertebrate nervous system are chemical, electrical synapses have also been identified in several brain regions. This type of synapse is dependent on the formation of gap junctions between the connected neurons and allows for the bi-directional passage of current between cells.

  • Most electrical synapses so far described are established between inhibitory neurons. Moreover, these synapses are largely formed between cells that belong to the same functional class. However, the possibility that exceptions to this rule exist has not been discarded and constitutes an active area of research.

  • The voltage change observed in a neuron when current is injected into another cell to which it is coupled by electrical synapses — the coupling coefficient — varies greatly, and usually averages 2–10%, although it can be as large as 40%. Several factors such as the conductance of single gap-junction channels, the total number of channels, their distance from the somata, and the input resistance of the cells can influence the coupling coefficient and, therefore, the efficacy of electrical synapses.

  • The existence of electrical synapses has several functional implications. For example, they could contribute to the spike synchronization of different cell populations and in the coordination of inhibitory postsynaptic potentials. Electrical synapses could also contribute to the oscillatory activity described in networks of inhibitory neurons. However, functional studies of electrical synapses are in their infancy and constitute one of the priorities in this rapidly moving field.

Abstract

Although gap junctions were first demonstrated in the mammalian brain about 30 years ago, the distribution and role of electrical synapses have remained elusive. A series of recent reports has demonstrated that inhibitory interneurons in the cerebral cortex, thalamus, striatum and cerebellum are extensively interconnected by electrical synapses. Investigators have used paired recordings to reveal directly the presence of electrical synapses among identified cell types. These studies indicate that electrical coupling is a fundamental feature of local inhibitory circuits and suggest that electrical synapses define functionally diverse networks of GABA-releasing interneurons. Here, we discuss these results, their possible functional significance and the insights into neuronal circuit organization that have emerged from them.

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Figure 1: Gap junctions between dendrites of inhibitory neocortical interneurons.
Figure 2: Electrical coupling between a pair of fast-spiking (FS) GABA interneurons.
Figure 3: Gap junctions are established between parvalbumin-containing interneurons.
Figure 4: Low-pass filter properties of signal transmission between electrically coupled neurons.
Figure 5: GABA interneurons can be connected by both electrical and chemical synapses.
Figure 6: Functional implications of electrical synapses in interneuron networks.

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Acknowledgements

Research support was from the National Eye Institute.

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Authors and Affiliations

  1. Department of Comparative Medicine, Stanford University School of Medicine, 300 Pasteur Drive, Stanford, 94305–5330, CA, USA

    Mario Galarreta & Shaul Hestrin

  2. Mario Galarreta

  3. Shaul Hestrin

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DATABASE LINKS

Cx32

Cx36

Cx43

Cx47

Glossary

ASYMMETRICAL SYNAPSES

Synaptic contacts in which the postsynaptic thickening is wider than the presynaptic one. They are thought to comprise largely excitatory connections. Symmetrical synapses, in contrast, are characterized by pre- and postsynaptic thickenings of roughly similar widths and are thought to be inhibitory. In the cortex, only inhibitory neurons receive asymmetric (excitatory) synapses at their somata.

SPIKE-FREQUENCY ADAPTATION

A decrease in the rate of action potentials fired by a neuron under prolonged depolarization.

PARVALBUMIN

A calcium-binding protein that can act as an endogenous buffer in certain neurons.

COUPLING COEFFICIENT

The ratio between the voltage change observed in the non-injected and the injected neurons.

INPUT RESISTANCE

The voltage change elicited by the injection of current into a cell divided by the amount of current injected.

ELECTROTONIC DISTANCE

In classical terms, it is defined as the anatomical distance between a channel or a synapse and the recording site, divided by the length constant (the distance at which signal amplitude decreases to 37% of its original amplitude).

LOW-PASS FILTER

A filter that suppresses all frequencies above a certain point known as the cutoff frequency.

MEMBRANE TIME CONSTANTS

These describe the time course of voltage changes in neurons. A small time constant means that the membrane potential can change rapidly.

AFTERHYPERPOLARIZATION

The membrane hyperpolarization that follows the occurrence of an action potential.

CROSS-CORRELOGRAM

A plot of the temporal relationship of events occurring in different cells. A peak near zero implies that there is no lag between the events.

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Galarreta, M., Hestrin, S. Electrical synapses between Gaba-Releasing interneurons. Nat Rev Neurosci 2, 425–433 (2001). https://doi.org/10.1038/35077566

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