Cortical GABA interneurons in neurovascular coupling: Relays for subcortical vasoactive pathways

Journal of Neuroscience

Volumn 24, Issue 41, 2004, Pages 8940-8949

  Cauli, Bruno ^a   Tong, Xin Kang ^b   Rancillac, Armelle ^a   Serluca, Nella ^b   Lambolez, Bertrand ^a   Rossier, Jean ^a   Hamel, Edith ^b  

^a CNRS   (France)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Brain microcirculation; Cerebral blood flow; Neocortex; Neuropeptide Y; Nitric oxide; Somatostatin; Vasoactive intestinal peptide

Indexed keywords

ACETYLCHOLINE; BIOCYTIN; CHOLINERGIC RECEPTOR; LAMININ; NEUROPEPTIDE Y; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE; SEROTONIN; SEROTONIN RECEPTOR; SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN CORTEX; BRAIN SLICE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GABAERGIC SYSTEM; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; INTERNEURON; MICROVASCULARIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASOCONSTRICTION; VASOMOTOR REFLEX;

ANIMALS; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; CYTOPLASM; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; LYSINE; MICROCIRCULATION; MUSCLE, SMOOTH, VASCULAR; NEUROPEPTIDE Y; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RECEPTORS, NEUROPEPTIDE; SIGNAL TRANSDUCTION; SOMATOSTATIN; VASOACTIVE INTESTINAL PEPTIDE; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASODILATION; VASODILATOR AGENTS;

EID: 5644289368     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3065-04.2004     Document Type: Article

References (52)

1. Abounader R, Hamel E (1997) Associations between Neuropeptide Y nerve terminals and intraparenchymal microvessels in rat and human cerebral cortex. J Comp Neurol 388:444-453.
2. Abounader R, Elhusseiny A, Cohen Z, Olivier A, Stanimirovic D, Quirion R, Hamel E (1999) Expression of neuropeptide Y receptors mRNA and protein in human brain vessels and cerebromicrovascular cells in culture. J Cereb Blood Flow Metab 19:155-163.
3. Bao L, Kopp J, Zhang X, Xu Z-QD, Zhang L-F, Wong H, Walsh J, Hokfelt T (1997) Localization of neuropeptide Y Y1 receptors in cerebral blood vessels. Proc Natl Acad Sci USA 94:12661-12666.
4. Bayraktar T, Staiger JF, Acsady L, Cozzari C, Freund TF, Zilles K (1997) Co-localization of vasoactive intestinal polypeptide, gamma-aminobutyric acid and choline acetyltransferase in neocortical interneurons of the adult rat. Brain Res 757:209-217.
5. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical non-pyramidal cells. J Neurosci 17:3894-3906.
6. Cauli B, Porter JT, Tsuzuki K, Lambolez B, Rossier J, Quenet B, Audinat E (2000) Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci USA 97:6144-6149.
7. Chédotal A, Cozzari C, Faure MP, Hartman BK, Hamel E (1994a) Distinct choline acetyltransferase (ChAT) and vasoactive intestinal polypeptide (VIP) bipolar neurons project to local blood vessels in the rat cerebral cortex. Brain Res 646:181-193.
8. Chédotal A, Umbriaco D, Descarries L, Hartman BK, Hamel E (1994b) Neurovascular relationships of cholinergic and VIPergic nerve terminals in rat cerebral cortex. J Comp Neurol 343:57-71.
9. Cohen Z, Bonvento G, Lacombe P, Hamel E (1996) Serotonin in the regulation of brain microcirculation. Prog Neurobiol 50:335-362.
10. Curtis SB, Hewitt J, Yakubovitz S, Anzarut A, Hsiang YN, Buchan AM (2000) Somatostatin receptor subtype expression and function in human vascular tissue. Am J Physiol Heart Circ Physiol 278:H1815-H1822.
11. Descarries L, Mechawar N (2000) Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central system. Prog Brain Res 125:27-47.
12. Dutour A, Kumar U, Panetta R, Ouafik L, Fina F, Sasi R (1998) Expression of somatostatin receptor subtypes in human brain tumors. Int J Cancer 76:620-627.
13. Eckenstein F, Baughman RW (1984) Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature 309:153-155.
14. Elhusseiny A, Hamel E (2000) Muscarinic-but not nicotinic-acetylcholine receptors mediate a nitric oxide-dependent dilation in brain cortical arterioles. J Cereb Blood Flow Metab 20:298-305.
15. Estrada C, DeFelipe J (1998) Nitric oxide-producing neurons in the neocortex: morphological and functional relationship with intraparenchymal microvasculature. Cereb Cortex 8:193-203.
16. 1R) in rat cerebral blood vessels: relation to PACAP and VIP containing nerves. J Cereb Blood Flow Metab 20:1205-1214.
17. Ferezou I, Cauli B, Hill EL, Rossier J, Hamel E, Lambolez B (2002) 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J Neurosci 22:7389-7397.
18. Fergus A, Lee KS (1997) GABAergic regulation of cerebral microvascular tone in the rat. J Cereb Blood Flow Metab 17:992-1003.
19. Fergus A, Jin Y, Thai Q-A, Kassell NF, Lee KS (1996) Tonic protein kinase C-mediated vasoconstriction is unmasked when nitric oxide synthase is inhibited in cerebral microvessels. Neuroscience 74:927-934.
20. Foehring RC, van Brederode JFM, Kinney GA, Spain WJ (2002) Serotonergic modulation of supragranular neurons in rat sensorimotor cortex. J Neurosci 22:8238-8250.
21. Hamel E (2004) Cholinergic modulation of the cortical microvascular bed. Prog Brain Res 145:171-178.
22. Harder DR, Zhang C, Gebremedhin D (2002) Astrocytes function in matching blood flow to metabolic activity. News Physiol Sci 16:27-31.
23. Harrison RV, Harel N, Panesar J, Mount RJ (2002) Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex. Cereb Cortex 12:225-233.
24. Iadecola C (2002) Intrinisc signals and functional brain mapping: caution, blood vessels at work. Cereb Cortex 12:223-224.
25. Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev 5:347-360.
26. Iadecola C, Arneric SP, Baker HD, Tucker LW, Reis DJ (1987) Role of local neurons in cerebrocortical vasodilation elicited from cerebellum. Am J Physiol 252:R1082-R1091.
27. Iadecola C, Beitz AJ, Renno W, Xu XMB, Zhang F (1993) Nitric oxide synthase-containing neural processes on large cerebral arteries and cerebral microvessels. Brain Res 606:148-155.
28. Kawaguchi Y (1997) Selective cholinergic modulation of cortical GABAergic cell subtypes. J Neurophysiol 78:1743-1747.
29. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
30. Krimer LS, Muly III EC, Williams GV, Goldman-Rakic PS (1998) Dopaminergic regulation of cerebral cortical microcirculation. Nat Neurosci 1:286-289.
31. Kubota Y, Hattori R, Yui Y (1994) Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649:159-173.
32. Lambolez B, Audinat E, Bochet P, Crépel F, Rossier J (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9:247-258.
33. Lauritzen M, Gold L (2003) Brain function and neurophysiological correlates of signals used in functional neuroimaging. J Neurosci 23:3972-3980.
34. Lindauer U, Megow K, Matsuda H, Dirnagl U (1999) Nitric oxide: a modulator, but not a mediator, of neurovascular coupling in rat somatosensory cortex. Am J Physiol 277:H799-H811.
35. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157.
36. Long JB, Rigamonti DD, Dosaka K, Kraimer JM, Martinez-Arizala A (1992) Somatostatin causes vasoconstriction, reduces blood flow and increases vascular permeability in the rat central nervous system. J Pharmacol Exp Ther 260:1425-1432.
37. Martin J-L, Feinstein DL, Yu N, Sorg O, Rossier C, Magistretti PJ (1992) VIP receptor subtypes in mouse cerebral cortex: evidence for a differential localization in astrocytes, microvessels and synaptosomal membranes. Brain Res 587:1-12.
38. Moro V, Badaut J, Springhetti V, Edvinsson L, Seylaz J, Lasbennes F (1995) Regional study of the co-localization of neuronal nitric oxide synthase with muscarinic receptors in the rat cerebral cortex. Neuroscience 69:797-805.
39. Nakai K, Naka Y, Yokote H, Ikatura T, Imai H, Komai N, Maeda T (1989) Vascular "sphincter" and microangioarchitecture in the central nervous system: constriction of intraparenchymal blood vessels following a treatment of vasoconstrictive neurotransmitter. Scanning Microsc 3:337-341.
40. Paspalas CD, Papadopoulos GC (1998) Ultrastructural evidence for combined action of noradrenaline and vasoactive intestinal polypeptide upon neurons, astrocytes, and blood vessels of the rat cerebral cortex. Brain Res Bull 45:247-259.
41. Paspalas CD, Papadopoulos GC (2001) Serotoninergic afferents preferentially innervate distinct subclasses of peptidergic interneurons in the rat visual cortex. Brain Res 891:158-167.
42. Porter JT, Cauli B, Tsuzuki K, Lambolez B, Rossier J, Audinat E (1999) Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J Neurosci 19:5228-5235.
43. Raichle ME (1998) Behind the scenes of functional brain imaging: a historical and physiological perspective. Proc Natl Acad Sci USA 95:765-772.
44. Sagher O, Zhang X-Q, Szeto W, Thai QA, Jin Y, Kassell NF, Lee KS (1993) Live computerized videomicroscopy of cerebral microvessels in brain slices. J Cereb Blood Flow Metab 13:676-682.
45. Tong XK, Hamel E (2000) Basal forebrain nitric oxide synthase (NOS)-containing neurons project to microvessels and NOS neurons in the rat neocortex: cellular basis for cortical blood flow regulation. Eur J Neurosci 12:2769-2780.
46. Tuor UI, Kelly PAT, Edvinsson L, McCulloch J (1990) Neuropeptide Y and the cerebral circulation. J Cereb Blood Flow Metab 10:591-601.
47. Vaucher E, Linville D, Hamel E (1997) Cholinergic basal forebrain projections to nitric oxide synthase-containing neurons in the rat cerebral cortex. Neuroscience 79:827-836.
48. Vaucher E, Tong X-K, Cholet N, Lantin S, Hamel E (2000) GABA neurons provide a rich input to microvessels but not nitric oxide neurons in the rat cerebral cortex: a means for direct regulation of local cerebral blood flow. J Comp Neurol 421:161-171.
49. Viollet C, Lanneau C, Faivre-Bauman A, Zhang J, Djordjijevic D, Loudes C, Gardette R, Kordon C, Epelbaum J (1997) Distinct patterns of expression and physiological effects of sst1 and sst2 receptor subtypes in mouse hypothalamic neurons and astrocytes in culture. J Neurochem 68:2273-2280.
50. Woolsey TA, Rovainen CM, Cox SB, Henegar MH, Liang GE, Liu D, Moskalenko YE, Sui J, Wei L (1996) Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. Cereb Cortex 6:647-660.
51. Yaksh TL, Wang J-Y, Go VLW (1987) Cortical vasodilatation produced by vasoactive intestinal polypeptide (VIP) and by physiological stimuli in the cat. J Cereb Blood Flow Metab 7:315-326.
52. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann K-A, Pozzan T, Carmignoto G (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43-50.