Classification of NPY-Expressing Neocortical Interneurons

Journal of Neuroscience - Tập 29 Số 11 - Trang 3642-3659 - 2009
Anastassios Karagiannis1,2, Thierry Gallopin1, Csaba Dávid3, Demian Battaglia4,5, H Geoffroy1, Jean Rossier1, Elizabeth M. C. Hillman6, Kathleen S. Rockland3, Bruno Cauli1,2
1NDC - Neurobiologie et diversité cellulaire (ESPCI, 10 Rue Vauquelin 75231 PARIS CEDEX 05 - bat.E / F 4ème étage - France)
2NPA - Neurobiologie des processus adaptatifs (bat. B , 4è, 5è, 6è étages 9 Quai Saint-Bernard - BP case1 75252 PARIS CEDEX 05 - France)
3Institute of Anatomy and Cell Biology (Department of Neuroanatomy, D-79001 Freiburg, Germany. - Germany)
4Bernstein CenterComputational Neuroscience, (D-37073 Göttingen, - Germany)
5NPSM - Neurophysique et physiologie du système moteur (45 Rue des Saints-Pères 75270 PARIS CEDEX 06 - France)
6Department of Biomedical Engineering, (351L Engineering Terrace, 1210 Amsterdam Avenue, New York, NY 10027, USA - United States)

Tóm tắt

Neuropeptide Y (NPY) is an abundant neuropeptide of the neocortex involved in numerous physiological and pathological processes. Because of the large electrophysiological, molecular, and morphological diversity of NPY-expressing neurons their precise identity remains unclear. To define distinct populations of NPY neurons we characterized, in acute slices of rat barrel cortex, 200 cortical neurons of layers I–IV by means of whole-cell patch-clamp recordings, biocytin labeling, and single-cell reverse transcriptase-PCR designed to probe for the expression of well established molecular markers for cortical neurons. To classify reliably cortical NPY neurons, we used and compared different unsupervised clustering algorithms based on laminar location and electrophysiological and molecular properties. These classification schemes confirmed that NPY neurons are nearly exclusively GABAergic and consistently disclosed three main types of NPY-expressing interneurons. (1) Neurogliaform-like neurons exhibiting a dense axonal arbor, were the most frequent and superficial, and substantially expressed the neuronal isoform of nitric oxide synthase. (2) Martinotti-like cells characterized by an ascending axon ramifying in layer I coexpressed somatostatin and were the most excitable type. (3) Among fast-spiking and parvalbumin-positive basket cells, NPY expression was correlated with pronounced spike latency. By clarifying the diversity of cortical NPY neurons, this study establishes a basis for future investigations aiming at elucidating their physiological roles.

Từ khóa


Tài liệu tham khảo

10.1002/(SICI)1096-9861(19971124)388:3<444::AID-CNE7>3.0.CO;2-0

10.1126/science.6136091

10.1152/jn.91094.2008

Aoki, 1989, Neuropeptide Y in the cerebral cortex and the caudate-putamen nuclei: ultrastructural basis for interactions with GABAergic and non-GABAergic neurons, J Neurosci, 9, 4333, 10.1523/JNEUROSCI.09-12-04333.1989

10.1038/nrn2402

10.1073/pnas.012481899

10.1016/S0006-8993(00)02285-X

10.1073/pnas.94.23.12661

Baraban, 1997, Knock-out mice reveal a critical antiepileptic role for neuropeptide Y, J Neurosci, 17, 8927, 10.1523/JNEUROSCI.17-23-08927.1997

10.1016/0896-6273(93)90086-7

10.1016/S0006-8993(97)00218-7

10.1002/(SICI)1096-9861(20000508)420:3<291::AID-CNE2>3.0.CO;2-H

10.1038/78809

10.1152/jn.00283.2003

10.1016/S0306-4522(97)00131-0

Cauli, 1997, Molecular and physiological diversity of cortical nonpyramidal cells, J Neurosci, 17, 3894, 10.1523/JNEUROSCI.17-10-03894.1997

10.1073/pnas.97.11.6144

10.1523/JNEUROSCI.3065-04.2004

10.1126/science.3945815

10.1016/0306-4522(90)90091-H

10.1002/ana.10158

Christophe, 2002, Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons, J Neurophysiol, 88, 1318, 10.1152/jn.2002.88.3.1318

Chu, 2003, Synaptic interactions of late-spiking neocortical neurons in layer 1, J Neurosci, 23, 96, 10.1523/JNEUROSCI.23-01-00096.2003

10.1002/jnr.1092

10.1016/0166-2236(90)90185-D

Dacey, 1988, Vasomotor responses of rat intracerebral arterioles to vasoactive intestinal peptide, substance P, neuropeptide Y, and bradykinin, J Cereb Blood Flow Metab, 8, 254, 10.1038/jcbfm.1988.56

10.1111/j.1460-9568.2007.05496.x

10.1073/pnas.88.17.7797

10.1113/jphysiol.2008.155580

Demeulemeester, 1988, Heterogeneity of GABAergic cells in cat visual cortex, J Neurosci, 8, 988, 10.1523/JNEUROSCI.08-03-00988.1988

Demeulemeester, 1991, Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex, Exp Brain Res, 84, 538, 10.1007/BF00230966

10.1523/JNEUROSCI.0134-07.2007

10.1023/A:1003291218707

10.1093/cercor/bhj126

10.1093/cercor/8.3.193

Férézou, 2002, 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons, J Neurosci, 22, 7389, 10.1523/JNEUROSCI.22-17-07389.2002

10.1093/cercor/bhl104

Fisher RA Yates F (1963) Statistical tables for biological, agricultural and medical research (Oliver and Boyd, Edinburgh).

10.1016/j.neuron.2007.09.012

10.1016/j.neuron.2008.01.034

10.1002/(SICI)1096-9861(19970127)377:4<465::AID-CNE1>3.0.CO;2-0

10.1038/47029

10.1093/cercor/bhj081

10.1073/pnas.0803125105

10.1038/47035

10.1016/j.neuron.2008.03.003

10.1371/journal.pcbi.0030156

10.1093/cercor/7.4.347

10.3389/neuro.05.003.2007

10.1177/34.11.2877022

10.1152/jn.00493.2006

10.1126/science.287.5451.273

Haj-Dahmane, 1997, Calcium-activated cation nonselective current contributes to the fast afterdepolarization in rat prefrontal cortex neurons, J Neurophysiol, 78, 1983, 10.1152/jn.1997.78.4.1983

10.1152/jn.01079.2005

10.2307/2346830

10.1093/cercor/bhn138

10.1073/pnas.81.20.6526

Hendry, 1984, Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex, J Neurosci, 4, 2497, 10.1523/JNEUROSCI.04-10-02497.1984

Hestrin, 1996, Morphology and physiology of cortical neurons in layer I, J Neurosci, 16, 5290, 10.1523/JNEUROSCI.16-17-05290.1996

10.1002/cne.21395

Hodgkin, 1948, The local electric changes associated with repetitive action in a non-medullated axon, J Physiol, 107, 165, 10.1113/jphysiol.1948.sp004260

10.1002/cne.903040205

10.1093/cercor/11.7.666

10.1002/(SICI)1097-0029(19990615)45:6<401::AID-JEMT7>3.0.CO;2-Q

10.1038/nn1909

10.1523/JNEUROSCI.4814-03.2004

Kawaguchi, 1993, Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex, J Neurophysiol, 69, 416, 10.1152/jn.1993.69.2.416

Kawaguchi, 1995, Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex, J Neurosci, 15, 2638, 10.1523/JNEUROSCI.15-04-02638.1995

Kawaguchi, 1993, Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex, J Neurophysiol, 70, 387, 10.1152/jn.1993.70.1.387

Kawaguchi, 1996, Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex, J Neurosci, 16, 2701, 10.1523/JNEUROSCI.16-08-02701.1996

10.1016/0006-8993(94)91060-X

10.1002/cne.902800305

10.1002/cne.902800306

10.1016/0896-6273(92)90164-9

Lee, 2005, Immunocytochemical localization of nitric oxide synthase-containing neurons in mouse and rabbit visual cortex and co-localization with calcium-binding proteins, Mol Cells, 19, 408, 10.1016/S1016-8478(23)13187-6

10.1523/JNEUROSCI.0661-06.2006

MacQueen JB (1967) Proceedings of the fifth Berkeley symposium in mathematical statistics and probability Some methods of classification and analysis of multivariate observations (University of California, Berkeley, CA), Vol 1, pp 281–297.

McCormick, 1985, Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex, J Neurophysiol, 54, 782, 10.1152/jn.1985.54.4.782

10.1016/0006-8993(84)90763-7

Mountcastle, 1969, Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination, J Neurophysiol, 32, 452, 10.1152/jn.1969.32.3.452

10.1016/j.tins.2006.05.004

Oláh, 2007, Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex, Front Neural Circuits, 1, 4, 10.3389/neuro.04.004.2007

10.1046/j.1460-9568.1998.00367.x

Porter, 1999, Selective excitation of subtypes of neocortical interneurons by nicotinic receptors, J Neurosci, 19, 5228, 10.1523/JNEUROSCI.19-13-05228.1999

10.1152/jn.00794.2006

10.1152/jn.90396.2008

10.1523/JNEUROSCI.1135-05.2005

10.1038/1092

10.1016/0006-8993(92)91439-L

10.1016/0377-0427(87)90125-7

Schubert, 2001, Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex, J Neurosci, 21, 3580, 10.1523/JNEUROSCI.21-10-03580.2001

Schubert, 2003, Cell type-specific circuits of cortical layer IV spiny neurons, J Neurosci, 23, 2961, 10.1523/JNEUROSCI.23-07-02961.2003

10.1523/JNEUROSCI.1431-05.2005

10.1016/S0006-8993(00)02136-3

Somogyi, 1984, Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material, J Neurosci, 4, 2590, 10.1523/JNEUROSCI.04-10-02590.1984

10.1046/j.1460-9568.2002.02048.x

10.1093/cercor/bhh029

10.1007/BF00374949

10.1038/nn1618

10.1073/pnas.0707204104

Tamás, 1997, Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex, J Physiol, 500, 715, 10.1113/jphysiol.1997.sp022054

10.1126/science.1082053

10.1111/j.1460-9568.2004.03719.x

10.1113/jphysiol.2005.089250

10.1002/cne.21504

10.1111/j.1460-9568.2005.03989.x

10.1159/000124141

10.1093/cercor/bhm056

10.1093/cercor/12.4.395

10.1113/jphysiol.2004.073353

10.2307/2282967

Yan, 1997, Morphological diversity of nitric oxide synthesising neurons in mammalian cerebral cortex, J Hirnforsch, 38, 165

10.1093/cercor/6.3.524

Zaitsev AV Povysheva NV Gonzalez-Burgos G Rotaru D Fish KN Krimer LS Lewis DA (2008) Interneuron diversity in layers 2–3 of monkey prefrontal cortex. Cereb Cortex, Advance online publication. Retrieved March 5, 2009. doi:10.1093/cercor/bhn198 .

Zhou, 1996, Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties, J Neurophysiol, 76, 651, 10.1152/jn.1996.76.2.651

Zhou, 1999, Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex, J Neurophysiol, 82, 2989, 10.1152/jn.1999.82.6.2989