Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons

Examination of cholecystokinin-immunoreactive cells in the rat frontal cortex revealed the presence in layers I-VI of a non-uniform population ranging in size from small to large. All were also immunoreactive for GABA. The most commonly observed dendritic form of the small cells were bipolar or bitufted although some were multipolar and demonstrated vasoactive intestinal polypeptide and in a few case calretinin immunoreactivity. The large cells were multipolar or bitufted and lacked expression of vasoactive intestinal polypeptide and calretinin immunoreactivity but occasionally showed calbindin D28k immunoreactivity. Therefore, the cholecystokinin-immunoreactive cells could be divided into two distinct subpopulations depending on their chemistry and morphology. Our previous studies showed that GABAergic cells in the neocortex could be classified into at least three chemically different subgroups: (1) parvalbumin-containing cells; (2) somatostatin-containing cells (most of them also contain calbindin D28k); and (3) vasoactive intestinal polypeptide- and/or calretinin-containing cells. The present results indicated that the small cholecystokinin-immunoreactive non-pyramidal cells constitute a subset of the vasoactive intestinal polypeptide- and/or calretinin-containing cortical GABAergic cells. The large cells remain to be categorized.

[1]  P. Somogyi,et al.  Synaptic connections, axonal and dendritic patterns of neurons immunoreactive for cholecystokinin in the visual cortex of the cat , 1986, Neuroscience.

[2]  J. Lund,et al.  Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics , 1993, The Journal of comparative neurology.

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

[4]  Y. Kawaguchi,et al.  Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. , 1993, Journal of neurophysiology.

[5]  E G Jones,et al.  Neuropeptide-containing neurons of the cerebral cortex are also GABAergic. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. Roberts.  An Atlas of Normal Developmental Roentgen Anatomy , 1988 .

[7]  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.

[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]  M. Tohyama,et al.  Cholecystokinin-8-like immunoreactivity in the pre- and post-central gyri of the human cerebral cortex , 1984, Brain Research.

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

[11]  J. Burgunder,et al.  Cortical neurons expressing the cholecystokinin gene in the rat: Distribution in the adult brain, ontogeny, and some of their projections , 1990, The Journal of comparative neurology.

[12]  T. Hökfelt,et al.  Cholecystokinin in Cortico‐striatal Neurons in the Rat: Immunohistochemical Studies at the Light and Electron Microscopical Level , 1994, The European journal of neuroscience.

[13]  J. Parnavelas,et al.  Extensive co-existence of neuropeptides in the rat visual cortex , 1987, Brain Research.

[14]  V. Trudeau,et al.  Expression of cholecystokinin mRNA in corticothalamic projecting neurons: a combined fluorescence in situ hybridization and retrograde tracing study in the ventrolateral thalamus of the rat. , 1995, Brain research. Molecular brain research.

[15]  G. Papadopoulos,et al.  VIP‐ and CCK‐like‐immunoreactive neurons in the hedgehog (Erinaceus europaeus) and Sheep (Ovis aries) brain , 1987, The Journal of comparative neurology.

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

[17]  R. R. Sturrock,et al.  Problems of the Keimbahn: New Work on Mammalian Germ Cell Lineage , 1985 .

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

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

[20]  J. Kuźnicki,et al.  Antibody Recognition of Calcium‐Binding Proteins Depends on Their Calcium‐Binding Status , 1996, Journal of neurochemistry.

[21]  G. Uhl,et al.  Cholecystokinin octapeptide-like immunoreactivity: histochemical localization in rat brain. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. Batini,et al.  Cytoplasmic calcium buffer, calbindin-D28k, is regulated by excitatory amino acids. , 1993, Neuroreport.

[23]  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.

[24]  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.

[25]  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.

[26]  D. Lewis,et al.  Postnatal development of the cholecystokinin innervation of monkey prefrontal cortex , 1993, The Journal of comparative neurology.

[27]  A. Peters,et al.  Cholecystokinin-like immunoreactive neurons in rat cerebral cortex , 1983, Neuroscience.

[28]  E. Jones,et al.  Cholecystokinin-immunoreactive neurons in rat and monkey cerebral cortex make symmetric synapses and have intimate associations with blood vessels. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Y. Kubota,et al.  Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. , 1993, Journal of neurophysiology.