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Review
. 2008 Jul;9(7):557-68.
doi: 10.1038/nrn2402.

Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex

Petilla Interneuron Nomenclature Group  1 ; Giorgio A Ascoli, Lidia Alonso-Nanclares, Stewart A Anderson, German Barrionuevo, Ruth Benavides-Piccione, Andreas Burkhalter, György Buzsáki, Bruno Cauli, Javier Defelipe, Alfonso Fairén, Dirk Feldmeyer, Gord Fishell, Yves Fregnac, Tamas F Freund, Daniel Gardner, Esther P Gardner, Jesse H Goldberg, Moritz Helmstaedter, Shaul Hestrin, Fuyuki Karube, Zoltán F Kisvárday, Bertrand Lambolez, David A Lewis, Oscar Marin, Henry Markram, Alberto Muñoz, Adam Packer, Carl C H Petersen, Kathleen S Rockland, Jean Rossier, Bernardo Rudy, Peter Somogyi, Jochen F Staiger, Gabor Tamas, Alex M Thomson, Maria Toledo-Rodriguez, Yun Wang, David C West, Rafael Yuste
Affiliations
Review

Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex

Petilla Interneuron Nomenclature Group et al. Nat Rev Neurosci. 2008 Jul.

Abstract

Neuroscience produces a vast amount of data from an enormous diversity of neurons. A neuronal classification system is essential to organize such data and the knowledge that is derived from them. Classification depends on the unequivocal identification of the features that distinguish one type of neuron from another. The problems inherent in this are particularly acute when studying cortical interneurons. To tackle this, we convened a representative group of researchers to agree on a set of terms to describe the anatomical, physiological and molecular features of GABAergic interneurons of the cerebral cortex. The resulting terminology might provide a stepping stone towards a future classification of these complex and heterogeneous cells. Consistent adoption will be important for the success of such an initiative, and we also encourage the active involvement of the broader scientific community in the dynamic evolution of this project.

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Figures

Figure 1
Figure 1. Somatic and dendritic morphology: shape and fine structure
Human cerebral cortex sections stained by NADPH-diaphorase histochemistry reveal key features of somatic and dendritic morphology. a–h | Examples of soma shape and dendritic arborization polarity. Somata can be fusiform (a–c), polygonal (d), round (g), triangular (h) or shapes that are not described by any of these terms (e,f). Dendritic arborization can be termed monopolar (a), bitufted (b), bipolar (c) or multipolar (d). i–k | Higher-magnification images showing structural details of the dendrites. Dendrites can be fairly regular and aspiny (i), irregular and spiny (j; arrows indicate spines) or beaded and aspiny (k; arrows indicate beads). Scale bars: a–d (shown in d): 50 µm; e–h (shown in f): 20 µm; i–k (shown in k): 10 µm. Images supplied by Javier DeFelipe.
Figure 2
Figure 2. Basic morphological features that describe neuronal branching
Dendritic and axonal processes can be quantified with many different metrics. These measurements are illustrated schematically to show the properties of the complex structures that can be captured. Representative exemplars of branches that would give increasing numerical values are shown for each metric. Although some metrics can be understood with little explanation (such as taper), others are not immediately intuitive and must be defined mathematically (such as fractal dimension). Sholl analysis yields a plot rather than a single value. In some cases, cortical interneurons can be distinguished from pyramidal cells and from each other using a combination of these metrics. Images supplied by Adam Packer.
Figure 3
Figure 3. Axonal morphology and synaptic structure
A | An example of a dense plexus of highly branched axons: a neurogliaform cell in the rat somatosensory cortex. The soma and dendrites are shown in black and the axon is shown in red. B | A double-bouquet cell from the cat primary visual cortex. The soma and dendrites are shown in red and the axon is shown in black. Note the characteristic horsetail-like axonal distribution. C | Morphological characteristics of a layer-3 large basket cell from the cat primary visual cortex. In this three-dimensional computer reconstruction, the soma and dendrites are shown in red and the axon is shown in black. The axon arborized profusely in the lower half of layer 3 (black boutons) and had a lateral extent of 1.1 mm from the parent soma (indicated by the asterisk). In addition, two axon collaterals descended into layers 5 and upper 6, each of which provided a small tuft (dark gray boutons). In layer 4, only a few boutons (light gray) were found. The total length of the axon was 44.053 mm, and it had 5,373 boutons. Typically, large basket cell boutons establish multiple axo-somatic contacts on other neurons. D | Fine structure of an axon revealed in a photomicrograph, showing terminal boutons (indicated by arrow heads) and boutons en passant (indicated by arrows). The image was obtained by staining a section of human cerebral cortex using NADPH-diaphorase histochemistry. E | Correlated light and electron microscopy of autapses. Ea | A myelinated axonal branch (labelled ‘ax’) gives rise to six terminal boutons (four of which, a1, a2, a3 and a5, are labelled) that are apposed to the dendrite (labelled ‘d’). Eb | Three of the terminal boutons shown in Ea emerge from the myelinated axonal trunk (ax) and establish synapses (indicated by the arrows) on successive dendritic beads, as illustrated at higher magnification in Ec–e. Scale bars: Ea: 10 µm; Eb: 1 µm; Ec–e (shown in Ec): 0.3 µm. D, dorsal; M, medial; PIA, pia mater; WM, white matter. Part A modified, with permission, from REF. © (2003) American Association for the Advancement of Science. Part B reproduced, with permission, from REF. © (1998) Society for Neuroscience. Part C courtesy of Alex s. Ferecskó. Part D supplied by Javier DeFelipe. Part E reproduced, with permission, from REF. © (1997) Society for Neuroscience.
Figure 4
Figure 4. Functional characterization of interneurons
a,b | Electrophysiological protocols used to measure neurons’ after hyperpolarization (AHP) and sag responses. Somatic current injection (bottom trace in both plots) and recorded membrane voltage (top traces) reveal an AHP (a) and a sag response (b). c–f | Diverse interneuron subclasses translate distinct patterns of activity into unique Ca2+ signals. The warmth of the colour reflects the magnitude of the Ca2+ accumulations. Axon terminals (indicated by the small black arrows) are positioned adjacent to dendrites to illustrate the spatial arrangement of synaptic activation, which can be in clusters or alone. c | A schematic of dendritic Ca2+ dynamics during a single action potential (left), a subthreshold excitatory postsynaptic potential (EPSP) (centre) and EPSP/action-potential coupling (right) in the dendrites of a multipolar perisoma-targeting fast-spiking cell from neocortical layer 2/3. Note that Ca2+ influx during single action potentials is proximally restricted. During subthreshold synaptic activation, convergent inputs activate dendritic subunits whereas individual inputs cause microdomains of Ca2+ accumulation. During EPSP/action-potential coupling, spikes propagate specifically to synaptically activated synaptic compartments where IA currents are inactivated. d | A schematic of a neocortical layer-2/3 calretinin-positive irregular-spiking interneuron stimulated as in c. The Ca2+ dynamics of bipolar irregular-spiking cells resemble fast-spiking cells, except that they lack Ca2+ microdomains. e | Dendritic Ca2+ signals in a layer-2/3 bitufted cell during action-potential backpropagation (left) and repetitive subthreshold (centre) and suprathreshold (right) activation of a single synapse. The multiple arrowheads on the individual schematic axonal terminals represent repetitive activation of a single synapse. f | Dendritic Ca2+ signals in a layer-5 rebound-spiking dendrite-targeting interneuron. In burst mode (left), synaptic activation (top trace) or somatic current injection (bottom trace) generates rebound spikes and highest Ca2+ signals at distal dendrites, where low-voltage-activated Ca2+ channels are clustered. In tonic mode (right), globally propagating Na+-based action potentials triggered either synaptically (top trace) or by somatic current injection (bottom trace) cause uniform Ca2+ accumulations. Excitation that is subthreshold for rebound-spike or action-potential generation does not cause Ca2+ influx (centre). Parts a and b reproduced from REF. . Parts c–f reproduced, with permission, from REF. © (2005) Elsevier Science.
Figure 5
Figure 5. Petilla terminology: types of firing patterns
Cortical GABAergic interneurons display a vast repertoire of discharge responses. These samples are representative of the most common responses to standardized intrasomatic step-current injections in the rat neocortex. The features of firing patterns in response to step-onset, organized in columns, include bursts, delays and continuous firing, which is neither burst nor delayed. Steady-state patterns, displayed in rows, can be fast spiking, non-adapting non-fast spiking, adapting, irregular spiking, intrinsic burst firing or accelerating. Fast spiking neurons can also display a stuttering or ‘Morse-code-like’ discharge that is characterized by high-frequency spike clusters that are intermingled with unpredictable periods of silence for a wide range of long, sustained, somatic-current injections. Blank areas of the table and boxes containing only scale bars correspond to firing patterns that have not yet been characterized in neocortical interneurons. The scale bar at the top left refers to the traces in the first four rows; the scale bars in the fifth and sixth rows refers to the traces in the fifth and sixth rows, respectively.
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