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  • Review Article
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Interneurons unbound

Nature Reviews Neuroscience volume 2, pages 11–23 (2001)Cite this article

Abstract

Local-circuit, γ-aminobutyric acid-releasing inhibitory interneurons of the hippocampus and cortex have traditionally been considered as the regulators of principal neuron activity — the yin to the excitatory yang. Recent evidence indicates that, in addition to that role, their network connectivity and the properties of their intrinsic voltage-gated currents are finely tuned to permit inhibitory interneurons to generate and control the rhythmic output of large populations of both principal cells and other populations of inhibitory interneurons. This review brings together recently described properties and emerging principles of interneuron function that indicate a much more complex role for these cells than just providers of inhibition.

Key Points

  • Interneurons have been largely considered as simple providers of inhibition. However, recent evidence indicates that their role is more complex. One particular example of this is the fact that interneurons can generate and control the rhythmic output of large populations of both principal cells and other populations of inhibitory interneurons.

  • Interneurons have been classified under different criteria, such as their anatomy, their neurochemical content, their firing patterns and other cellular properties. However, all of these classifications have obtained limited success. One alternative classification that has become increasingly common and that may pave the way towards a general understanding of interneuron subtypes and the rules of their connectivity is based on the nature of the excitatory input received by interneurons, in combination with their inhibitory output.

  • Interneurons possess different types of glutamate receptor, which endow principal neuron–interneuron communication with specific properties. The rapid kinetic properties of α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA)-receptor-mediated excitatory synaptic potentials (EPSPs) can detect coincident firing of multiple presynaptic inputs. The smaller and slower kainate receptor EPSPs are most effective during temporal summation at lower frequencies of activation.

  • Another factor that influences interneuron function is the pattern of expression of voltage-gated ion channels. Interneurons possess Ca2+ and Na+ channels that endow them with properties different from principal cells. However, the differential expression of K+ channels constitutes the clearest example of the importance of voltage-dependent conductances for interneuron function. In particular, K+ conductances control fast interneuron spiking and the temporal precision with which EPSPs trigger action potentials in interneurons.

  • Communication among interneurons is both chemical (through γ-aminobutyrate (GABA)-releasing synapses) and electrical (through gap junctions). These two forms of communication show distinct polarities, timing and short-term dynamics and, therefore, are likely to have different functions. Nevertheless, neuronal synchronization within interneuronal networks is likely to result from a synergistic effect of both electrical and chemical coupling.

  • By virtue of their extensive interconnections, interneurons form distinct networks that have important roles in shaping the activity of the central nervous system. One common property of interneuron networks is the generation of oscillatory rhythmic activity. Computational and empirical approaches have shown that intrinsic conductances, properties of inhibitory synaptic transmission, and interneuronal connectivity through gap junctions dictate the nature of the oscillatory activity.

  • To understand the role of interneurons in a particular function of the nervous system, one must understand the nature of the afferent input, the specific roles of voltage-gated conductances, the types of interneuronal signalling, and the anatomical identity of the cell types of interest. This information will allow us to build more precise models and to ask clearer questions about the roles of specific inhibitory interneurons in generating or modulating particular brain functions.

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Figure 1: Domain-specific innervation of hippocampal interneurons.
Figure 2: Ca2+-permeable AMPA receptors mediate fast synaptic transmission in interneurons.
Figure 3: Fast-spiking and precision timing are controlled by intrinsic K+ conductances.
Figure 4: GABA-mediated chemical transmission and gap junction-mediated electrical transmission.
Figure 5: Interneurons and networks.

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Authors and Affiliations

  1. Laboratory of Cellular and Molecular Neurophysiology, National Institute of Child Health and Human Development, Room 5A72, Building 49, 49 Convent Drive, Bethesda, 20892-4495, Maryland, USA

    Chris J. McBain & André Fisahn

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ENCYCLOPEDIA OF LIFE SCIENCES

Cells of the nervous system

Dendrites

GABAA receptors

Oscillatory neural networks

Glossary

FEEDFORWARD ACTIVATION

In the feedforward regulatory system, afferent volleys directly activate the inhibitory neuron.

FEEDBACK ACTIVATION

In the feedback system, an excitatory input discharges the principal cells, whose excitatory output is fed back to the inhibitory cells through recurrent axon collaterals.

RECURRENT COLLATERALS

Axons from cells that project back to the neurons that originally activated them.

PRINCIPAL CELLS

In the hippocampus, this term refers to both the pyramidal cells of the hippocampus proper and the granule cells of the dentate gyrus.

ELECTROTONIC PROPERTIES

Term used to describe the passive properties of the cell membrane; that is, the properties not influenced by the voltage-dependent properties of the neuron.

RECTIFICATION

The property whereby current through a channel does not flow with the same ease from the inside as that from the outside. In inward rectification, for instance, current into the cell flows more easily than it flows out of the cell through the same population of channels.

CURRENT–VOLTAGE RELATIONSHIP

A plot of the changes of ionic current as a function of membrane voltage.

BASKET CELLS

Interneurons that send their axons to the cell body of the postsynaptic cell, surrounding it with a structure akin to a basket.

QUANTAL AMPLITUDE

The amplitude of the synaptic response elicited by a single vesicle of a transmitter.

DECAY TIME CONSTANT

The initial decay of an EPSP can usually be fit by a single exponential function. The time constant derived from this fit describes how quickly an EPSP decays.

GLUR2FLIP

Two splice variants of AMPA receptors known as flip and flop have been characterized. They differ in their response to glutamate, their distribution in the brain and their developmental expression.

COINCIDENCE DETECTION

The ability to sense the simultaneous occurrence of synaptic activity at different points of the same cell.

STRATUM LUCIDUM

The site of termination of the mossy fibres from the dentate gyrus onto CA3 neurons of the hippocampus.

POLYAMINES

Organic compounds that contain two or more amino groups. Putrescine, spermine and spermidine are prime examples.

ASSOCIATIONAL INPUTS

The projections from CA3 neurons to other CA3 cells on the same side of the brain. Commissural inputs are CA3–CA3 connections between the two hemispheres.

TEMPORAL SUMMATION

The way in which non-simultaneous synaptic events add in time. One of the basic elements of synaptic integration

AFTERHYPERPOLARIZATION

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

PERTUSSIS TOXIN

The causative agent of whooping cough, pertusis toxin causes the persistent activation of Gi proteins by catalyzing the ADP-ribosylation of the α subunit.

INPUT RESISTANCE

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

CUT FREQUENCY

The frequency at which a train of suprathreshold stimuli fails to elicit an action potential on every pulse. See also definition of 'low-pass filter'.

ALVEUS

Bundle of fibres formed by the efferent hippocampal axons. The alveus constitutes the first part of the fornix.

GAP JUNCTIONS

Cellular junctions that allow the free passage of current and small molecules through non-selective channels called connexons.

PHASE LAG

The time delay with which one rhythmic activity follows another of the same frequency.

LOW-PASS FILTER

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

NESTING OF OSCILLATIONS

The simultaneous occurrence of two phase-locked rhythms with different frequencies.

SPIKE-FREQUENCY ADAPTATION

The cessation of action-potential firing upon constant depolarization.

EMERGENT PROPERTY

A collective network property that is not a property of any one element forming the network (that is to say, the whole is more than the sum of its parts).

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McBain, C., Fisahn, A. Interneurons unbound. Nat Rev Neurosci 2, 11–23 (2001). https://doi.org/10.1038/35049047

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