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Dendritic integration of excitatory synaptic input

Abstract

A fundamental function of nerve cells is the transformation of incoming synaptic information into specific patterns of action potential output. An important component of this transformation is synaptic integration — the combination of voltage deflections produced by a myriad of synaptic inputs into a singular change in membrane potential. There are three basic elements involved in integration: the amplitude of the unitary postsynaptic potential, the manner in which non-simultaneous unitary events add in time (temporal summation), and the addition of unitary events occurring simultaneously in separate regions of the dendritic arbor (spatial summation). This review discusses how passive and active dendritic properties, and the functional characteristics of the synapse, shape these three elements of synaptic integration.

Key Points

  • Neurons receive a plethora of synaptic inputs that are widely spread across their dendritic arbours. This spatial distribution, together with the cable properties of dendrites could cause a pronounced location-dependent variability in the integration properties of synaptic inputs, unless the filtering properties of dendrites are countered.

  • Although theoretical analyses predict a marked location dependence for the integration of spatially segregated synaptic input, evidence indicates that the dendrites of some cell types can counteract the influence of filtering on the three main elements of synaptic integration — unitary EPSP amplitude, and temporal and spatial summation.

  • As a result of countering the filtering properties of dendrites, synaptic integration is essentially independent of input location. Three broad categories of cellular properties are involved in the normalization of synaptic integration — neuron morphology, active properties of the membrane and synaptic mechanisms.

  • Neuron morphology can reduce the location dependence of synaptic integration but its effect cannot completely counteract the filtering effects of dendrites, indicating that the contribution of other cellular properties to linearization is more important.

  • The active properties of the dendritic membrane are more effective than neuron morphology in reducing the location dependence of integration. Active dendritic conductances endow neurons with the ability to produce both linear and nonlinear interactions between synaptic inputs. However, their exact effect will depend on the specific spatio-temporal characteristics of the input.

  • Changes in synaptic conductance are the primary mechanism for reducing location dependence of integration in CA1 neurons. The precise nature of the synaptic change is unknown but it is likely to involve an increase in the number of release sites per terminal and increases in the number of synaptic receptors.

  • The location independence of integration has several functional benefits. For example, it allows a neuron to use Hebbian synaptic mechanisms to store information. Similarly, it could provide a mechanism for the linear encoding of information known to occur in several brain systems by allowing cells that receive spatially divergent patterns of connections from a homogeneous population of neurons to integrate the incoming information as part of the same class of input.

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Figure 1: The filtering effects of dendrites should be accompanied by location-dependent synaptic integration.
Figure 2: Synaptic integration in CA1 pyramidal neurons is independent of location.
Figure 3: EPSC-shaped current injections show that the passive morphology of CA1 pyramidal neurons does not fully counter location-dependent synaptic variability.
Figure 4: Other mechanisms such as active membrane and synaptic properties are required to completely counter location-dependent synaptic variability.

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ENCYCLOPEDIA OF LIFE SCIENCES

Dendrites

Glossary

CABLE FILTERING

Dendrites have been commonly modelled as cables and the flow of current between two points of a dendrite has been usually assumed to decay as a result of filtering along the process.

HEBBIAN PROCESSES

Plastic processes that require temporal coincidence between incoming synaptic activity and postsynaptic depolarization.

AXIAL RESISTANCE

The resistance to the flow of ionic current along an axon or a dendrite. Axial resistance decreases as a function of the radius of the process and increases as a function of its length.

MEMBRANE CAPACITANCE

The cell membrane separates and stores electrical charge, thereby producing a relatively large electrical capacitance, which increases as a function of membrane area.

MEMBRANE CONDUCTANCE

The sum of all of the ionic conductances of the membrane. It is the reciprocal of the membrane resistance.

TEMPORAL-INTEGRATION MODE

Firing of action potentials in response to the summation of temporally dispersed synaptic activity. The synaptic input at the soma has small amplitude and long duration.

COINCIDENCE-DETECTION MODE

In this mode, a cell fires action potentials in response to the simultaneous arrival of a small number of usually large amplitude, short duration inputs.

QUANTAL CURRENT

The current elicited by the transmitter released from a single synaptic vesicle.

QUANTAL CONTENT

The number of quanta released per action potential.

CAGED GLUTAMATE

An inactive derivative of glutamate that can be transformed into the active transmitter, usually by photolysis of the precursor. It provides an efficient means for the spatially restricted application of glutamate.

MINIMAL STIMULATION TECHNIQUES

Methods to elicit transmitter release from a few (ideally one) synaptic contacts.

EPSP HALF-WIDTH

The duration of an EPSP at the point at which its amplitude is half of the peak value.

DECAY TIME CONSTANTS

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

ISOPOTENTIALITY

The degree to which the dendritic compartments are all at the same potential.

TIME INTEGRAL

By accounting for the charge stored in the capacitance of the cells, the time integral of the EPSC relates more to the steady-state voltage attenuation and is therefore much less affected by dendritic filtering.

MAUTHNER CELLS

A bilateral pair of brainstem neurons that receive acoustic information and trigger an escape response characteristic of fish.

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.

FLOP VARIANT OF AMPA RECEPTORS

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

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Magee, J. Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1, 181–190 (2000). https://doi.org/10.1038/35044552

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