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  • Review Article
  • Published:

Neocortical cell classes are flexible entities

Key Points

Four main types of neocortical neurons.

Early research identified four types of neocortical neurons on the basis of their firing patterns: regular-spiking; intrinsically bursting; fast-rhythmic bursting; and fast-spiking. Although this classification scheme has heuristic value, it is an oversimplification. Some researchers favour the idea of further subdividing these neuronal types to account for the variety of responses that are seen in different preparations, whereas others champion the idea that neocortical neurons are flexible entities that can convert from one firing pattern to others.

Transitions of firing patterns between neuronal types.

Early classification of neocortical neurons aimed to incorporate neuronal types with similar anatomical and electrophysiological properties into clear-cut classes. But neither the anatomy nor the physiology seem to be compatible with this classification. Neurons of a given class are not restricted to specific areas or layers of the cortex, and manipulations such as subtle changes in membrane potential can affect the firing properties of single neurons.

Roles in normal and pathological states.

The different proportions of neuronal types in the cortex of behaving animals, compared with cortical tissue in vitro or in animals under anaesthesia, might explain the preferential role of certain cell classes in some functional states of the brain, such as the different brain states of vigilance, their associated brain oscillations, synaptic plasticity, conscious states, and pathological conditions such as epilepsy.

  • Natural states of vigilance

  • Brain rhythms during waking and sleep states

  • Synaptic plasticity

  • Correlations between cortical neuronal activities and conscious states

  • Role of different cortical neurons in seizures

Conclusion.

I conclude that the firing patterns of the four main neocortical neuronal classes are not inflexible, but can change in the same neuron from one pattern to another in response to slight changes in the membrane potential that occur naturally during shifts in brain states. Data on the cellular mechanisms that underlie these changes might assist in determining the role of different cell classes in normal and pathological states.

Abstract

In studies on preparations in which spontaneous activity is significantly reduced or negligible, the properties of different cortical neuronal classes seem to be inflexible. But intracellular studies in behaving animals have led to the conclusion that firing patterns can be transformed from one type into another by slight changes in the membrane potential during shifts in the state of vigilance. Also, the incidence of various neuronal types in wakeful animals is different from that reported in vitro or under anaesthesia. The variation in firing pattern and incidence of cellular classes might shed light on the role of the different neuronal types across the waking–sleep cycle and related oscillations, during synaptic plasticity and consciousness, and during the development of paroxysmal states.

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Figure 1: Four neuronal types in the neocortex, and changes in firing patterns with shifts in membrane potential.
Figure 2: Transformation of intrinsically bursting into regular-spiking firing pattern.
Figure 3: Selectively increased firing of cortical local-circuit (fast-spiking) neurons during saccades in rapid eye movement sleep.
Figure 4: Coalescence of low-frequency (spindle) and fast (gamma) rhythms by the slow sleep oscillation.
Figure 5: Synaptic plasticity induced by low-frequency stimuli mimicking sleep spindles.
Figure 6: Progressively increasing depolarization during cortically evoked augmenting responses in a fast-rhythmic-bursting neuron, leading to paroxysmal facilitation.
Figure 7: Thalamocortical neurons are inhibited during cortically generated spike–wave seizures, and exhibit phasic inhibitory postsynaptic potentials but not spike bursts.

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Acknowledgements

I thank previous Ph.D. students (D. Contreras and F. Grenier) and present collaborators and postdoctoral fellows (I. Timofeev, S. Crochet and Y. Cissé) for their participation in unpublished experiments that are mentioned in this article. I also thank T. J. Sejnowski, M. Bazhenov, A. Destexhe and W. W. Lytton for their collaboration in experimental and modelling studies. Personal work is supported by the Canadian Institutes for Health Research, Natural Sciences and Engineering Research Council of Canada, Human Frontier Science Program, and National Institutes of Health of the United States.

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Glossary

ANTIDROMIC

This term describes an action potential travelling from the axon terminal towards the cell body.

ORTHODROMIC

This term describes an action potential travelling away from the cell body down the axon.

ADAPTATION

Also referred to as accommodation, this term describes cessation of spike firing despite constant depolarization above threshold.

SACCADE

A rapid eye movement (with speeds of up to 800 degrees per second) that brings the point of maximal visual acuity — the fovea — to the image of interest. Saccades are also present during rapid eye movement sleep.

SEMANTIC MEMORY

The recollection of factual information independent of the specific episodes in which that information was acquired.

SPIKE–WAVE COMPLEX

EEG sequence consisting of 'spike' (during which cortical neurons fire) and 'wave' (during which cortical neurons are silent).

HYPSARRHYTHMIA

An electroencephalic abnormality that is characterized by random, high-voltage slow waves and spikes, which arise from multiple foci and spread through the cerebral cortex.

INPUT RESISTANCE

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

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Steriade, M. Neocortical cell classes are flexible entities. Nat Rev Neurosci 5, 121–134 (2004). https://doi.org/10.1038/nrn1325

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