Three distinct families of GABAergic neurons in rat visual cortex.

In the cortex inhibition is mediated predominantly by GABAergic interneurons. Although all of these neurons use the same neurotransmitter, studies in the rat frontal cortex have shown that they are molecularly and physiologically diverse. It is not known whether similar subgroups of GABAergic neurons exist in primary visual cortex and how these different inhibitory neurons are inserted into specific cortical circuits. We have used immunostaining with antibodies against gamma aminobutyric acid (GABA), parvalbumin (PV), calretinin (CR), somatostatin (SOM), calbindin (CB) and nitric oxide synthase (NOS) to probe for colocalization of known markers of GABAergic interneurons. The results show that the majority of PV (100%), SOM (89.8%) and CR (93.9%) staining neurons are GABA positive. PV immunoreactive neurons constitute a distinct group that show no overlap with CR, SOM and NOS expressing cells and only a minor overlap (5.3%) with CB. PV immunoreactive cells account for 50.8% of GABAergic neurons. A second group of SOM expressing neurons accounts for 16.9% of GABAergic cells. None of these cells colocalize PV or CR, but 1.7% of SOM neurons stain for NOS and 86.3% show CB immunoreactivity. The third distinct group of CR expressing cells accounts for 17.0% of GABAergic neurons. All of these are PV, CB, SOM and NOS negative. CB expressing neurons represent a heterogeneous group that includes GABAergic and non-GABAergic cells. Our findings indicate that GABAergic neurons in rat area 17 are organized in at least three separate families that can be identified by the expression of PV, CR and SOM. These cells account for 84.9% of GABAergic neurons. These results extend previous observations in rat frontal agranular cortex and suggest that in visual cortex the inhibitory network is composed of similar cell types.

[1]  P. Somogyi A specific ‘axo-axonal’ interneuron in the visual cortex of the rat , 1977, Brain Research.

[2]  M. Herkenham Laminar organization of thalamic projections to the rat neocortex. , 1980, Science.

[3]  A. Peters,et al.  Chandelier cells in rat visual cortex , 1982, The Journal of comparative neurology.

[4]  P. Somogyi,et al.  Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat , 1983, Neuroscience.

[5]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[6]  P. Emson,et al.  Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  A. Sillito Functional Considerations of the Operation of GABAergic Inhibitory Processes in the Visual Cortex , 1984 .

[8]  P. Somogyi,et al.  Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin- immunoreactive material , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Alan Peters,et al.  Cellular components of the cerebral cortex , 1984 .

[10]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[11]  R. R. Sturrock,et al.  Cerebral Cortex, vol 1. Cellular Components of the Cerebral Cortex , 1985, Neurology.

[12]  A. Peters,et al.  The neuronal composition of area 17 of rat visual cortex. III. Numerical considerations , 1985, The Journal of comparative neurology.

[13]  D. Whitteridge,et al.  Synaptic connections of intracellularly filled clutch cells: A type of small basket cell in the visual cortex of the cat , 1985, The Journal of comparative neurology.

[14]  S. Hendry,et al.  Co-localization of GABA and neuropeptides in neocortical neurons , 1986, Trends in Neurosciences.

[15]  M. Celio,et al.  Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. , 1986, Science.

[16]  P. Somogyi,et al.  Evidence for interlaminar inhibitory circuits in the striate cortex of the cat , 1987, The Journal of comparative neurology.

[17]  Stanley J. Watson,et al.  The rat brain in stereotaxic coordinates (2nd edn) by George Paxinos and Charles Watson, Academic Press, 1986. £40.00/$80.00 (264 pages) ISBN 012 547 6213 , 1987, Trends in Neurosciences.

[18]  T. Kosaka,et al.  An aspect of the organizational principle of the γ-aminobutyric acidergic system in the cerebral cortex , 1987, Brain Research.

[19]  J. DeFelipe,et al.  GABA—Peptide Neurons of the Primate Cerebral Cortex , 1987 .

[20]  Alan Peters,et al.  GABA immunoreactive neurons in rat visual cortex , 1987, The Journal of comparative neurology.

[21]  G A Orban,et al.  Heterogeneity of GABAergic cells in cat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  A. Burkhalter,et al.  Intrinsic connections of rat primary visual cortex: Laminar organization of axonal projections , 1989, The Journal of comparative neurology.

[23]  C. Barnstable,et al.  Molecular determinants of GABAergic local-circuit neurons in the visual cortex , 1989, Trends in Neurosciences.

[24]  E. G. Jones,et al.  Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity , 1989, Brain Research.

[25]  E G Jones,et al.  Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[26]  G. Orban,et al.  Calbindin D-28K and parvalbumin immunoreactivity is confined to two separate neuronal subpopulations in the cat visual cortex, whereas partial coexistence is shown in the dorsal lateral geniculate nucleus , 1989, Neuroscience Letters.

[27]  M. Celio,et al.  Calbindin D-28k and parvalbumin in the rat nervous system , 1990, Neuroscience.

[28]  H. Gundersen,et al.  Unbiased stereological estimation of the number of neurons in the human hippocampus , 1990, The Journal of comparative neurology.

[29]  A. Hendrickson,et al.  Calcium‐binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex , 1990, The Journal of comparative neurology.

[30]  E. G. Jones,et al.  A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons , 1990, Neuroscience.

[31]  D. Jacobowitz,et al.  Immunocytochemical localization of calretinin in the forebrain of the rat , 1991, The Journal of comparative neurology.

[32]  A. Hendrickson,et al.  Distribution of the calcium-binding proteins parvalbumin and calbindin-D28k in the sensorimotor cortex of the rat , 1991, Neuroscience.

[33]  J. Rogers Immunohistochemical markers in rat brain: colocalization of calretinin and calbindin-D28k with tyrosine hydroxylase , 1992, Brain Research.

[34]  J. Rogers,et al.  Calretinin and calbindin-D28k in rat brain: Patterns of partial co-localization , 1992, Neuroscience.

[35]  J. Rogers Immunohistochemical markers in rat cortex: co-localization of calretinin and calbindin-D28k with neuropeptides and GABA , 1992, Brain Research.

[36]  H. Kimura,et al.  Histochemical mapping of nitric oxide synthase in the rat brain , 1992, Neuroscience.

[37]  U. Eysel,et al.  Network of GABAergic large basket cells in cat visual cortex (area 18): Implication for lateral disinhibition , 1993, The Journal of comparative neurology.

[38]  A. Burkhalter,et al.  Hierarchical organization of areas in rat visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  E. G. Jones,et al.  GABAergic neurons and their role in cortical plasticity in primates. , 1993, Cerebral cortex.

[40]  C. Beaulieu,et al.  Numerical data on neocortical neurons in adult rat, with special reference to the GABA population , 1993, Brain Research.

[41]  I. Blümcke,et al.  The calcium-binding protein calretinin is localized in a subset of interneurons in the rat cerebral cortex: a light and electron immunohistochemical study. , 1993, Journal fur Hirnforschung.

[42]  J. DeFelipe,et al.  Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. , 1993, Cerebral cortex.

[43]  R. Weinberg,et al.  Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA , 1993, Neuroscience Letters.

[44]  Mark J. West,et al.  New stereological methods for counting neurons , 1993, Neurobiology of Aging.

[45]  J. Parnavelas,et al.  The emergence of the cortical GABAergic neuron: with particular reference to some peptidergic subpopulations , 1993, Journal of neurocytology.

[46]  P. Somogyi,et al.  Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. , 1994, Journal of neurophysiology.

[47]  Y. Kubota,et al.  Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex , 1994, Brain Research.

[48]  M. Celio,et al.  Localization of calretinin in cells of layer I (Cajal-Retzius cells) of the developing cortex of the rat. , 1994, Brain research. Developmental brain research.

[49]  Y. Kang,et al.  Spatiotemporally differential inhibition of pyramidal cells in the cat motor cortex. , 1994, Journal of neurophysiology.

[50]  L. Benardo,et al.  Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro. , 1994, The Journal of physiology.

[51]  Françoise Condé,et al.  Local circuit neurons immunoreactive for calretinin, calbindin D‐28k or parvalbumin in monkey prefronatal cortex: Distribution and morphology , 1994, The Journal of comparative neurology.

[52]  J. Parnavelas,et al.  Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calcium-binding protein homogeneity in clonally related cortical neurons , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  S. L. Dun,et al.  Infrequent co-localization of nitric oxide synthase and calcium binding proteins immunoreactivity in rat neocortical neurons , 1994, Brain Research.

[54]  Y. Kawaguchi Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  P. Somogyi,et al.  Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus , 1995, The European journal of neuroscience.

[56]  Y. Kubota,et al.  Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  R. Coggeshall,et al.  Methods for determining numbers of cells and synapses: A case for more uniform standards of review , 1996, The Journal of comparative neurology.

[58]  A. Burkhalter,et al.  Different Balance of Excitation and Inhibition in Forward and Feedback Circuits of Rat Visual Cortex , 1996, The Journal of Neuroscience.

[59]  Andreas Burkhalter,et al.  Microcircuitry of forward and feedback connections within rat visual cortex , 1996, The Journal of comparative neurology.

[60]  G. Bertini,et al.  The chemical heterogeneity of cortical interneurons: Nitric oxide synthase vs. calbindin and parvalbumin immunoreactivity in the rat , 1996, Brain Research Bulletin.