Key Points
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Burst firing — the intermittent discharge of rapid action-potential sequences — is a prominent feature of many sensory neurons. Its functional role is not fully understood, in spite of the considerable progress that has been made in the past 20 years. This review draws together recent findings on the biophysical mechanisms of burst firing, its control through feedback from higher brain centres, and its potential role in sensory information transmission.
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In vitro studies and compartmental modelling demonstrate that bursting relies on intrinsic ionic mechanisms that couple the fast process of action potential generation to slower processes that govern burst occurrence and duration. In compact neurons, both these slow and fast mechanisms are located at the soma. In neurons with extensive dendritic structures, the fast and slow processes can also be distributed over the dendrites, leading to qualitatively different mechanisms of bursting.
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The occurrence of bursts does not only rely on strong excitation by sensory inputs and intrinsic cellular mechanisms. Bursts also seem to be gated by inputs from additional brain areas. In neurons of the mammalian thalamus for example, brainstem inputs convey information on the level of vigilance of the animal, and drowsiness or sleep states might result in large-scale synchronized bursting. By contrast, burst probability is low during wakefulness. Cortical feedback onto the same neurons, on the other hand, might be able to gate sensory-driven bursting during wakefulness.
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In the hindbrain of weakly electric fish, synchronized burst responses seem to be gated by the behavioural context of sensory stimuli. Spatially extended stimuli that mimic communication with conspecifics favour synchronized firing patterns and increase periodic (oscillatory) bursting. By contrast, spatially localized stimuli that mimic small prey lead to non-oscillatory responses with low burst probability. The shift between these two response modes can be explained by the level of activation of a spatially diffuse inhibitory feedback pathway, which is strongly activated only by large-scale stimuli.
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Support for a distinct role of bursts in sensory systems comes from two main sources. First, bursts can increase the reliability of synaptic transmission. At facilitating synapses, this presumably occurs through accumulation of Ca2+ in the presynaptic terminal during high frequency firing. At depressing synapses of the thalamocortical system, the silent period preceding bursts acts to relieve depression and so enhances synaptic efficacy. Second, bursts occur as responses to sensory stimulation in alert animals and carry distinct information about these stimuli. In some systems, bursts improve the signal-to-noise ratio of sensory responses. In others, such as the electrosensory system of weakly electric fish, bursts might be involved in the detection of specific, behaviourally relevant stimulus features.
Abstract
Neurons that fire high-frequency bursts of spikes are found in various sensory systems. Although the functional implications of burst firing might differ from system to system, bursts are often thought to represent a distinct mode of neuronal signalling. The firing of bursts in response to sensory input relies on intrinsic cellular mechanisms that work with feedback from higher centres to control the discharge properties of these cells. Recent work sheds light on the information that is conveyed by bursts about sensory stimuli, on the cellular mechanisms that underlie bursting, and on how feedback can control the firing mode of burst-capable neurons, depending on the behavioural context. These results provide strong evidence that bursts have a distinct function in sensory information transmission.
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Acknowledgements
We gratefully acknowledge the provision of figure material by J. Bastian, E. D'Angelo and B. Doiron. We also would like to thank L. Chen for help with electric field modelling, and B. Boudreau and D. Sparks for critically reading the manuscript. F.G. is an Alfred P. Sloan Fellow. Funding from NIMH.
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Glossary
- SLOW-WAVE SLEEP
-
A phase of the sleep cycle that is characterized by the appearance of slow oscillations in the electroencephalogram.
- COMPARTMENTAL MODELLING
-
A computer modelling technique that breaks a neuron down into small electrical compartments and can simulate the propagation of electrical signals inside the neuron and across its membrane surface.
- SOMATOSENSORY SYSTEM
-
The system that mediates the sensation of touch, temperature, pain and movement of the joints.
- VENTROBASAL COMPLEX OF THE THALAMUS
-
Subdivision of the thalamus that relays somatosensory information to the cortex.
- MICROSACCADES
-
Small and abrupt involuntary eye movements that occur during fixation of an object and last for only a brief period of time.
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Krahe, R., Gabbiani, F. Burst firing in sensory systems. Nat Rev Neurosci 5, 13–23 (2004). https://doi.org/10.1038/nrn1296
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DOI: https://doi.org/10.1038/nrn1296
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