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PMID: 18568015 Published · ppublish English Journal Article Review

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

Nature reviews. Neuroscience ·Vol. 9 ·No. 7 ·2008-07-00 ·Pages 557-68

Petilla Interneuron Nomenclature Group, Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsáki G, Cauli B, Defelipe J, Fairén A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, Kisvárday ZF, Lambolez B, Lewis DA, Marin O, Markram H, Muñoz A, Packer A, Petersen CC, Rockland KS, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R

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.

MeSH Terms
Action Potentials Axons/ultrastructure Cerebral Cortex/cytology,metabolism Humans Interneurons/classification,cytology,metabolism Synapses/ultrastructure gamma-Aminobutyric Acid/metabolism
Chemicals
gamma-Aminobutyric Acid
Authors & Affiliations
40 authors, click to expand affiliations / ORCID
Petilla Interneuron Nomenclature Group
Molecular Neuroscience Department and Center for Neural Informatics, Structures, and Plasticity, Krasnow Institute for Advanced Study, George Mason University, MS2A1, 4400 University Drive, Fairfax, Virginia 22030, USA. [email protected];
Ascoli Giorgio A
Alonso-Nanclares Lidia
Anderson Stewart A
Barrionuevo German
Benavides-Piccione Ruth
Burkhalter Andreas
Buzsáki György
Cauli Bruno
Defelipe Javier
Fairén Alfonso
Feldmeyer Dirk
Fishell Gord
Fregnac Yves
Freund Tamas F
Gardner Daniel
Gardner Esther P
Goldberg Jesse H
Helmstaedter Moritz
Hestrin Shaul
Karube Fuyuki
Kisvárday Zoltán F
Lambolez Bertrand
Lewis David A
Marin Oscar
Markram Henry
Muñoz Alberto
Packer Adam
Petersen Carl C H
Rockland Kathleen S
Rossier Jean
Rudy Bernardo
Somogyi Peter
Staiger Jochen F
Tamas Gabor
Thomson Alex M
Toledo-Rodriguez Maria
Wang Yun
West David C
Yuste Rafael
References (99)
99 references, click to expand
  1. Measures for quantifying dendritic arborizations.
    Network. 2002 Aug;13(3):397-414 PMID: 12222821
  2. Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex.
    J Neurophysiol. 2007 Feb;97(2):1030-9 PMID: 17122314
  3. Ca2+ imaging of mouse neocortical interneurone dendrites: contribution of Ca2+-permeable AMPA and NMDA receptors to subthreshold Ca2+dynamics.
    J Physiol. 2003 Aug 15;551(Pt 1):67-78 PMID: 12844507
  4. Potentiation of cortical inhibition by visual deprivation.
    Nature. 2006 Sep 7;443(7107):81-4 PMID: 16929304
  5. Stereotypical bouton clustering of individual neurons in cat primary visual cortex.
    J Neurosci. 2007 Nov 7;27(45):12242-54 PMID: 17989290
  6. Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. I. Morphometric analysis.
    J Neurocytol. 1990 Apr;19(2):154-74 PMID: 2358827
  7. Synaptic mechanism of central inhibition.
    Prog Brain Res. 1968;22:67-85 PMID: 4297203
  8. The naming of neurons: applications of taxonomic theory to the study of cellular populations.
    Brain Behav Evol. 1975;12(1-2):75-96 PMID: 1104078
  9. Inhibitory CA1-CA3-hilar region feedback in the hippocampus.
    Science. 1994 Sep 16;265(5179):1722-4 PMID: 8085161
  10. 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons.
    J Neurosci. 2002 Sep 1;22(17):7389-97 PMID: 12196560
  11. Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat.
    J Neurosci. 1998 Jun 1;18(11):4255-70 PMID: 9592103
  12. Large-scale recording of neuronal ensembles.
    Nat Neurosci. 2004 May;7(5):446-51 PMID: 15114356
  13. Dendrites of classes of hippocampal neurons differ in structural complexity and branching patterns.
    J Comp Neurol. 1999 Nov 1;413(4):619-33 PMID: 10495447
  14. Site-specific and developmental expression of pannexin1 in the mouse nervous system.
    Eur J Neurosci. 2005 Jun;21(12):3277-90 PMID: 16026466
  15. The origin and specification of cortical interneurons.
    Nat Rev Neurosci. 2006 Sep;7(9):687-96 PMID: 16883309
  16. Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex.
    Cereb Cortex. 2004 Dec;14(12):1310-27 PMID: 15192011
  17. Properties of single axon excitatory postsynaptic potentials elicited in spiny interneurons by action potentials in pyramidal neurons in slices of rat neocortex.
    Neuroscience. 1995 Dec;69(3):727-38 PMID: 8596643
  18. Correlation between axonal morphologies and synaptic input kinetics of interneurons from mouse visual cortex.
    Cereb Cortex. 2007 Jan;17(1):81-91 PMID: 16467567
  19. Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents.
    J Physiol. 2000 Nov 15;529 Pt 1:205-13 PMID: 11080262
  20. The temporal and spatial origins of cortical interneurons predict their physiological subtype.
    Neuron. 2005 Nov 23;48(4):591-604 PMID: 16301176
  21. Redistribution of synaptic efficacy between neocortical pyramidal neurons.
    Nature. 1996 Aug 29;382(6594):807-10 PMID: 8752273
  22. Hippocampal CA1 interneurons: an in vivo intracellular labeling study.
    J Neurosci. 1995 Oct;15(10):6651-65 PMID: 7472426
  23. Dendritic GABA release depresses excitatory transmission between layer 2/3 pyramidal and bitufted neurons in rat neocortex.
    Neuron. 1999 Dec;24(4):979-88 PMID: 10624960
  24. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons.
    Nat Neurosci. 2000 Apr;3(4):366-71 PMID: 10725926
  25. Molecular taxonomy of major neuronal classes in the adult mouse forebrain.
    Nat Neurosci. 2006 Jan;9(1):99-107 PMID: 16369481
  26. Double bouquet cell in the human cerebral cortex and a comparison with other mammals.
    J Comp Neurol. 2005 Jun 13;486(4):344-60 PMID: 15846784
  27. Ca2+ imaging of mouse neocortical interneurone dendrites: Ia-type K+ channels control action potential backpropagation.
    J Physiol. 2003 Aug 15;551(Pt 1):49-65 PMID: 12844506
  28. Single-cell microarray analysis in hippocampus CA1: demonstration and validation of cellular heterogeneity.
    J Neurosci. 2003 May 1;23(9):3607-15 PMID: 12736331
  29. Neurons immunoreactive for vasoactive intestinal polypeptide in the rat primary somatosensory cortex: morphology and spatial relationship to barrel-related columns.
    J Comp Neurol. 2000 May 8;420(3):291-304 PMID: 10754503
  30. Robust correlations between action potential duration and the properties of synaptic connections in layer 4 interneurones in neocortical slices from juvenile rats and adult rat and cat.
    J Physiol. 2007 Apr 1;580(Pt 1):149-69 PMID: 17234697
  31. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro.
    Cereb Cortex. 2002 Sep;12(9):936-53 PMID: 12183393
  32. Interneuron Diversity series: Molecular and genetic tools to study GABAergic interneuron diversity and function.
    Trends Neurosci. 2004 Feb;27(2):90-7 PMID: 15102488
  33. Role of high-affinity receptors and membrane transporters in nonsynaptic communication and drug action in the central nervous system.
    Pharmacol Rev. 2000 Mar;52(1):63-89 PMID: 10699155
  34. The Ferrier Lecture, 1977. The neuron network of the cerebral cortex: a functional interpretation.
    Proc R Soc Lond B Biol Sci. 1978 May 16;201(1144):219-48 PMID: 27801
  35. Chandelier cells and epilepsy.
    Brain. 1999 Oct;122 ( Pt 10):1807-22 PMID: 10506085
  36. Synaptic alpha 5 subunit-containing GABAA receptors mediate IPSPs elicited by dendrite-preferring cells in rat neocortex.
    Cereb Cortex. 2008 Jun;18(6):1260-71 PMID: 17951598
  37. Ultrastructural study of gap junctions between dendrites of parvalbumin-containing GABAergic neurons in various neocortical areas of the adult rat.
    Neuroscience. 2003;120(1):5-20 PMID: 12849736
  38. NeuroMorpho.Org: a central resource for neuronal morphologies.
    J Neurosci. 2007 Aug 29;27(35):9247-51 PMID: 17728438
  39. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex.
    Science. 2000 Jan 14;287(5451):273-8 PMID: 10634775
  40. Massive autaptic self-innervation of GABAergic neurons in cat visual cortex.
    J Neurosci. 1997 Aug 15;17(16):6352-64 PMID: 9236244
  41. Combined Golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey.
    J Comp Neurol. 1981 Feb 1;195(4):547-66 PMID: 7462443
  42. AMPA receptor channels with long-lasting desensitization in bipolar interneurons contribute to synaptic depression in a novel feedback circuit in layer 2/3 of rat neocortex.
    J Neurosci. 2001 Oct 15;21(20):8062-71 PMID: 11588179
  43. GABAergic projections from the hippocampus to the retrosplenial cortex in the rat.
    Eur J Neurosci. 2007 Sep;26(5):1193-204 PMID: 17767498
  44. Back-propagating action potentials mediate calcium signalling in dendrites of bitufted interneurons in layer 2/3 of rat somatosensory cortex.
    J Physiol. 2001 Aug 15;535(Pt 1):17-31 PMID: 11507155
  45. Neocortical circuits: evolutionary aspects and specificity versus non-specificity of synaptic connections. Remarks, main conclusions and general comments and discussion.
    J Neurocytol. 2002 Mar-Jun;31(3-5):387-416 PMID: 12815255
  46. Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study.
    Eur J Neurosci. 1997 Mar;9(3):573-88 PMID: 9104599
  47. Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex.
    J Comp Neurol. 1985 Jan 15;231(3):364-84 PMID: 2981907
  48. Electrophysiology of a dendritic neuron model.
    Biophys J. 1962 Mar;2(2 Pt 2):145-67 PMID: 14490040
  49. Calcium microdomains in aspiny dendrites.
    Neuron. 2003 Nov 13;40(4):807-21 PMID: 14622584
  50. Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types.
    J Neurosci. 2005 Jul 20;25(29):6845-56 PMID: 16033894
  51. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat.
    J Neurosci. 1999 Jan 1;19(1):274-87 PMID: 9870957
  52. Heterogeneity of phasic cholinergic signaling in neocortical neurons.
    J Neurophysiol. 2007 Mar;97(3):2215-29 PMID: 17122323
  53. Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo.
    Nat Neurosci. 2004 Jan;7(1):41-7 PMID: 14634650
  54. Resonance, oscillation and the intrinsic frequency preferences of neurons.
    Trends Neurosci. 2000 May;23(5):216-22 PMID: 10782127
  55. Developmental changes in spinal motoneuron dendrites in neonatal mice.
    J Comp Neurol. 2005 Mar 14;483(3):304-17 PMID: 15682391
  56. Long-term synaptic plasticity in hippocampal feedback inhibitory networks.
    Prog Brain Res. 2008;169:241-50 PMID: 18394478
  57. The cerebral cortex of the mouse (a first contribution--the "acoustic" cortex).
    Somatosens Mot Res. 1992;9(1):3-36 PMID: 1317625
  58. GABAergic cell subtypes and their synaptic connections in rat frontal cortex.
    Cereb Cortex. 1997 Sep;7(6):476-86 PMID: 9276173
  59. Long-distance corticocortical GABAergic neurons in the adult monkey white and gray matter.
    J Comp Neurol. 2007 Dec 10;505(5):526-38 PMID: 17924571
  60. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids.
    Nature. 2004 Sep 16;431(7006):312-6 PMID: 15372034
  61. Molecular and physiological diversity of cortical nonpyramidal cells.
    J Neurosci. 1997 May 15;17(10):3894-906 PMID: 9133407
  62. The neuron classification problem.
    Brain Res Rev. 2007 Nov;56(1):79-88 PMID: 17582506
  63. Volume transmission in the CNS and its relevance for neuropsychopharmacology.
    Trends Pharmacol Sci. 1999 Apr;20(4):142-50 PMID: 10322499
  64. Neuronal diversity in GABAergic long-range projections from the hippocampus.
    J Neurosci. 2007 Aug 15;27(33):8790-804 PMID: 17699661
  65. In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):897-901 PMID: 1992481
  66. Anatomical organization of macaque monkey striate visual cortex.
    Annu Rev Neurosci. 1988;11:253-88 PMID: 3284442
  67. Identified sources and targets of slow inhibition in the neocortex.
    Science. 2003 Mar 21;299(5614):1902-5 PMID: 12649485
  68. Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modulation of interneurons.
    Cereb Cortex. 2007 May;17(5):1020-32 PMID: 16772311
  69. Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex.
    J Neurosci. 1998 Sep 1;18(17):6963-76 PMID: 9712665
  70. Postsynaptic calcium influx at single synaptic contacts between pyramidal neurons and bitufted interneurons in layer 2/3 of rat neocortex is enhanced by backpropagating action potentials.
    J Neurosci. 2004 Feb 11;24(6):1319-29 PMID: 14960603
  71. Cholinergic switching within neocortical inhibitory networks.
    Science. 1998 Aug 14;281(5379):985-8 PMID: 9703513
  72. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex.
    Cereb Cortex. 2003 Jan;13(1):25-32 PMID: 12466212
  73. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo.
    Nature. 2003 Feb 20;421(6925):844-8 PMID: 12594513
  74. Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum.
    J Neurosci. 1993 Nov;13(11):4908-23 PMID: 7693897
  75. Development of GABA innervation in the cerebral and cerebellar cortices.
    Nat Rev Neurosci. 2007 Sep;8(9):673-86 PMID: 17704810
  76. Interneuron Diversity series: Hippocampal interneuron classifications--making things as simple as possible, not simpler.
    Trends Neurosci. 2003 Oct;26(10):564-71 PMID: 14522150
  77. Long-term synaptic plasticity in hippocampal interneurons.
    Nat Rev Neurosci. 2007 Sep;8(9):687-99 PMID: 17704811
  78. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study.
    J Anat. 1959 Oct;93:420-33 PMID: 13829103
  79. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors.
    J Neurosci. 2007 Jul 18;27(29):7786-98 PMID: 17634372
  80. Salient features of synaptic organisation in the cerebral cortex.
    Brain Res Brain Res Rev. 1998 May;26(2-3):113-35 PMID: 9651498
  81. Functional maps of neocortical local circuitry.
    Front Neurosci. 2007 Oct 15;1(1):19-42 PMID: 18982117
  82. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study.
    Brain Res. 1968 Jul;9(2):268-87 PMID: 4175993
  83. Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex.
    Eur J Neurosci. 1998 Dec;10(12):3617-28 PMID: 9875341
  84. The blue brain project.
    Nat Rev Neurosci. 2006 Feb;7(2):153-60 PMID: 16429124
  85. Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting.
    J Physiol. 2004 Jul 15;558(Pt 2):465-78 PMID: 15146046
  86. Defined types of cortical interneurone structure space and spike timing in the hippocampus.
    J Physiol. 2005 Jan 1;562(Pt 1):9-26 PMID: 15539390
  87. Space matters: local and global dendritic Ca2+ compartmentalization in cortical interneurons.
    Trends Neurosci. 2005 Mar;28(3):158-67 PMID: 15749170
  88. Mobilizing the base of neuroscience data: the case of neuronal morphologies.
    Nat Rev Neurosci. 2006 Apr;7(4):318-24 PMID: 16552417
  89. The organization of area 18 in the monkey. A Golgi study.
    Anat Embryol (Berl). 1978 Sep 27;154(3):305-34 PMID: 101094
  90. Quantitative morphologic classification of layer 5 neurons from mouse primary visual cortex.
    J Comp Neurol. 2003 Jul 7;461(4):415-28 PMID: 12746859
  91. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat.
    J Physiol. 2004 Nov 15;561(Pt 1):65-90 PMID: 15331670
  92. Interneurons unbound.
    Nat Rev Neurosci. 2001 Jan;2(1):11-23 PMID: 11253355
  93. Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation.
    Neuroscience. 1993 May;54(2):347-60 PMID: 8336829
  94. Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs.
    Cereb Cortex. 2006 Feb;16(2):200-11 PMID: 15843627
  95. The organization of the visual cortex in the cat.
    J Anat. 1955 Jan;89(1):33-46 PMID: 14353795
  96. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus.
    J Neurosci. 1999 Nov 15;19(22):10082-97 PMID: 10559416
  97. Dendritic organization in the neurons of the visual and motor cortices of the cat.
    J Anat. 1953 Oct;87(4):387-406 PMID: 13117757
  98. Electrical coupling and neuronal synchronization in the Mammalian brain.
    Neuron. 2004 Feb 19;41(4):495-511 PMID: 14980200
  99. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features.
    J Neurophysiol. 2004 Jul;92(1):600-8 PMID: 15056678
Article Info
Journal
Nature reviews. Neuroscience
Abbr.
Nat Rev Neurosci
ISSN
1471-0048
DOI
10.1038/nrn2402
Email
[email protected]
Published
2008-07-00
Pages
557-68
Language
English
Region
England
NLM ID
100962781
PMCID
PMC2868386
Subset
IM
Grants
Medical Research Council · MC_U138197107 · United Kingdom
NINDS NIH HHS · R01 NS044820 · United States
NINDS NIH HHS · R01 NS044820-04 · United States
NINDS NIH HHS · R56 NS011862 · United States
Medical Research Council · G0000207 · United Kingdom
NINDS NIH HHS · R01 NS011862 · United States
NINDS NIH HHS · R56 NS011862-27A1 · United States
External Links
PubMed source DOI: 10.1038/nrn2402 PMC Full Text View journal details
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