Distinct receptors underlie glutamatergic signalling in inspiratory rhythm-generating networks and motor output pathways in neonatal rat

Journal of Physiology

Volumn 586, Issue 9, 2008, Pages 2357-2370

  Ireland, M F ^a   Lenal, F C ^a   Lorier, A R ^a,b   Loomes, D E ^a   Adachi, T ^a   Alvares, T S ^a   Greer, J J ^a   Funk, G D ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 5 TERT BUTYL 3 HYDROXY 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 5; GLUTAMATE RECEPTOR ANTAGONIST; KAINIC ACID; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PYRIMIDINE 2,4 DIONE; SUBSTANCE P; UBP 302;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREATHING MUSCLE; BREATHING RATE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EVOKED SPINAL CORD RESPONSE; IN VITRO STUDY; INSPIRATORY CAPACITY; NERVE POTENTIAL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN QUATERNARY STRUCTURE; RAT; RECEPTOR BINDING; RECEPTOR SENSITIVITY; RESPIRATORY DRIVE; RHYTHM; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON; SPINAL ROOT; SYNAPTIC TRANSMISSION; WHOLE CELL; AMPLITUDE MODULATION; BRAIN SLICE; BRAIN STEM; BREATHING MECHANICS; GLUTAMATERGIC SYNAPSE; INSPIRATORY RHYTHM; MEDULLA OBLONGATA; MOTONEURON; MOTOR SYSTEM; NERVE ROOT; SPINAL CORD;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; CELLS, CULTURED; EFFERENT PATHWAYS; GLUTAMIC ACID; INHALATION; MOTOR NEURONS; NERVE NET; RATS; RATS, WISTAR; RECEPTORS, AMPA; SIGNAL TRANSDUCTION;

EID: 42949122978     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2007.150532     Document Type: Article

References (61)

1. Aghajanian GK & Rasmussen K (1989). Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse 3, 331-338.
2. Alt A, Weiss B, Ogden AM, Knauss JL, Oler J, Ho K, Large TH & Bleakman D (2004). Pharmacological characterization of glutamatergic agonists and antagonists at recombinant human homomeric and heteromeric kainate receptors in vitro. Neuropharmacology 46, 793-806.
3. Bleakman D, Gates MR, Ogden AM & MacKowiak M (2002). Kainate receptor agonists, antagonists and allosteric modulators. Curr Pharm Des 8, 873-885.
4. Bleakman R, Schoepp DD, Ballyk B, Bufton H, Sharpe EF, Thomas K, Ornstein PL & Kamboj RK (1996). Pharmacological discrimination of GluR5 and GluR6 kainate receptor subtypes by
5. Bortolotto ZA, Clarke VR, Delany CM, Parry MC, Smolders I, Vignes M, Ho KH, Miu P, Brinton BT, Fantaske R, Ogden A, Gates M, Ornstein PL, Lodge D, Bleakman D & Collingridge GL (1999). Kainate receptors are involved in synaptic plasticity. Nature 402, 297-301.
6. Clarke VR, Ballyk BA, Hoo KH, Mandelzys A, Pellizzari A, Bath CP, Thomas J, Sharpe EF, Davies CH, Ornstein PL, Schoepp DD, Kamboj RK, Collingridge GL, Lodge D & Bleakman D (1997). A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389, 599-603.
7. Cossart R, Esclapez M, Hirsch JC, Bernard C & Ben-Ari Y (1998). GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1, 470-478.
8. Feldman JL & Del Negro CA (2006). Looking for inspiration: New perspectives on respiratory rhythm. Nat Rev Neurosci 7, 232-242.
9. Funk GD, Johnson SM, Smith JC, Dong XW, Lai J & Feldman JL (1997). Functional respiratory rhythm generating networks in neonatal mice lacking NMDAR1 gene. J Neurophysiol 78, 1414-1420.
10. Funk GD, Smith JC & Feldman JL (1993). Generation and transmission of respiratory oscillations in medullary slices: Role of excitatory amino acids. J Neurophysiol 70, 1497-1515.
11. Funk GD, Smith JC & Feldman JL (1995). Modulation of neural network activity in vitro by cyclothiazide, a drug that blocks desensitization of AMPA receptors. J Neurosci 15, 4046-4056.
12. Garcia Del Cano G, Millan LM, Gerrikagoitia I, Sarasa M & Matute C (1999). Ionotropic glutamate receptor subunit distribution on hypoglossal motoneuronal pools in the rat. J Neurocytol 28, 455-468.
13. Ge Q & Feldman JL (1998). AMPA receptor activation and phosphatase inhibition affect neonatal rat respiratory rhythm generation. J Physiol 509, 255-266.
14. Gray PA, Janczewski WA, Mellen N, McCrimmon DR & Feldman JL (2001). Normal breathing requires preBötzinger complex neurokinin-1 receptor-expressing neurons. Nat Neurosci 4, 927-930.
15. Gray PA, Rekling JC, Bocchiaro CM & Feldman JL (1999). Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBötzinger complex. Science 286, 1566-1568.
16. Greer JJ, Smith JC & Feldman JL (1991). Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J Physiol 437, 727-749.
17. Gryder DS & Rogawski MA (2003). Selective antagonism of GluR5 kainate-receptor-mediated synaptic currents by topiramate in rat basolateral amygdala neurons. J Neurosci 23, 7069-7074.
18. Guyenet PG & Wang H (2001). Pre-Bötzinger neurons with preinspiratory discharges 'in vivo'express NK1 receptors in the rat. J Neurophysiol 86, 438-446.
19. Hollmann M & Heinemann S (1994). Cloned glutamate receptors. Annu Rev Neurosci 17, 31-108.
20. 3H]ATPA: A high affinity ligand for GluR5 kainate receptors. Neuropharmacology 38, 1811-1817.
21. Huettner JE (1990). Glutamate receptor channels in rat DRG neurons: activation by kainate and quisqualate and blockade of desensitization by Con A. Neuron 5, 255-266.
22. Ireland MF, Noakes PG & Bellingham MC (2004). P2×7-like receptor subunits enhance excitatory synaptic transmission at central synapses by presynaptic mechanisms. Neuroscience 128, 269-280.
23. Janczewski WA & Feldman JL (2006). Distinct rhythm generators for inspiration and expiration in the juvenile rat. J Physiol 570, 407-420.
24. Kieval JZ, Hubert GW, Charara A, Pare JF & Smith Y (2001). Subcellular and subsynaptic localization of presynaptic and postsynaptic kainate receptor subunits in the monkey striatum. J Neurosci 21, 8746-8757.
25. Kitamura S & Sakai A (1982). A study on the localization of the sternocleidomastoid and trapezius motoneurons in the rat by means of the HRP method. Anat Rec 202, 527-536.
26. Krolo M, Stuth EA, Tonkovic-Capin M, Dogas Z, Hopp FA, Mccrimmon DR & Zuperku EJ (1999). Differential roles of ionotropic glutamate receptors in canine medullary inspiratory neurons of the ventral respiratory group. J Neurophysiol 82, 60-68.
27. Krolo M, Stuth EA, Tonkovic-Capin M, Hopp FA, Mccrimmon DR & Zuperku EJ (2000). Relative magnitude of tonic and phasic synaptic excitation of medullary inspiratory neurons in dogs. Am J Physiol Regulatory Integrative Comp Physiol 279, R639-R649.
28. Kullmann DM (2001). Presynaptic kainate receptors in the hippocampus: slowly emerging from obscurity. Neuron 32, 561-564.
29. Li P, Wilding TJ, Kim SJ, Calejesan AA, Huettner JE & Zhuo M (1999). Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature 397, 161-164.
30. Lindsay AD, Greer JJ & Feldman JL (1991). Phrenic motoneuron morphology in the neonatal rat. J Comp Neurol 308, 169-179.
31. Liu G, Feldman JL & Smith JC (1990). Excitatory amino acid-mediated transmission of inspiratory drive to phrenic motoneurons. J Neurophysiol 64, 423-436.
32. Liu QS, Xu Q, Arcuino G, Kang J & Nedergaard M (2004). Astrocyte-mediated activation of neuronal kainate receptors. Proc Natl Acad Sci U S A 101, 3172-3177.
33. Lorier AR, Huxtable AG, Robinson DM, Lipski J, Housley GD & Funk GD (2007). P2Y1 receptor modulation of the pre-Bötzinger complex inspiratory rhythm generating network in vitro. J Neurosci 27, 993-1005.
34. McCrimmon DR, Smith JC & Feldman JL (1989). Involvement of excitatory amino acids in neurotransmission of inspiratory drive to spinal respiratory motoneurons. J Neurosci 9, 1910-1921.
35. Mayer ML, Ghosal A, Dolman NP & Jane DE (2006). Crystal structures of the kainate receptor GluR5 ligand binding core dimer with novel GluR5-selective antagonists. J Neurosci 26, 2852-2861.
36. Mellen NM, Janczewski WA, Bocchiaro CM & Feldman JL (2003). Opioid-induced quantal slowing reveals dual networks for respiratory rhythm generation. Neuron 37, 821-826.
37. Miles GB, Parkis MA, Lipski J & Funk GD (2002). Modulation of phrenic motoneuron excitability by ATP: Consequences for respiratory-related output in vitro. J Appl Physiol 92, 1899-1910.
38. More JC, Nistico R, Dolman NP, Clarke VR, Alt AJ, Ogden AM, Buelens FP, Troop HM, Kelland EE, Pilato F, Bleakman D, Bortolotto ZA, Collingridge GL & Jane DE (2004). Characterisation of UBP296: A novel, potent and selective kainate receptor antagonist. Neuropharmacology 47, 46-64.
39. Nicholson C (1985). Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res 333, 325-329.
40. Olsen DP, Dunlap K & Jacob MH (2007). Kainate receptors and RNA editing in cholinergic neurons. J Neurochem 101, 327-341.
41. Onimaru H & Homma I (2003). A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23, 1478-1486.
42. Paarmann I, Frermann D, Keller BU & Hollmann M (2000). Expression of 15 glutamate receptor subunits and various splice variants in tissue slices and single neurons of brainstem nuclei and potential functional implications. J Neurochem 74, 1335-1345.
43. Pace RW, MacKay DD, Feldman JL & Del Negro CA (2007). Inspiratory bursts in the preBötzinger complex depend on a calcium-activated non-specific cation current linked to glutamate receptors in neonatal mice. J Physiol 582, 113-125.
44. Pagliardini S, Adachi T, Ren J, Funk GD & Greer JJ (2005). Fluorescent tagging of rhythmically active respiratory neurons within the pre-Bötzinger complex of rat medullary slice preparations. J Neurosci 25, 2591-2596.
45. Palmer CL, Cotton L & Henley JM (2005). The molecular pharmacology and cell biology of a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Pharmacol Rev 57, 253-277.
46. Partin KM, Patneau DK, Winters CA, Mayer ML & Buonanno A (1993). Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11, 1069-1082.
47. Paternain AV, Rodriguez-Moreno A, Villarroel A & Lerma J (1998). Activation and desensitization properties of native and recombinant kainate receptors. Neuropharmacology 37, 1249-1259.
48. Patneau DK, Mayer ML, Jane DE & Watkins JC (1992). Activation and desensitization of AMPA/kainate receptors by novel derivatives of willardiine. J Neurosci 12, 595-606.
49. Pelletier JC, Hesson DP, Jones KA & Costa AM (1996). Substituted 1,2-dihydrophthalazines: Potent, selective and non-competitive inhibitors of the AMPA receptor. J Medicalchem 39, 343-346.
50. Petralia RS & Wenthold RJ (1992). Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 318, 329-354.
51. Robinson D & Ellenberger H (1997). Distribution of N-methyl-D-aspartate and non-N-methyl-D-aspartate glutamate receptor subunits on respiratory motor and premotor neurons in the rat. J Comp Neurol 389, 94-116.
52. Rodriguez-Moreno A, Herreras O & Lerma J (1997). Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19, 893-901.
53. +] of confocally imaged respiratory center neurons in on-line-calibrated newborn rat brainstem slices. J Neurosci 26, 11870-11880.
54. Sallert M, Malkki H, Segerstrale M, Taira T & Lauri SE (2007). Effects of the kainate receptor agonist ATPA on glutamatergic synaptic transmission and plasticity during early postnatal development. Neuropharmacology 52, 1354-1365.
55. Smith JC, Ellenberger HH, Ballanyi K, Richter DW & Feldman JL (1991). Pre-Bötzinger complex: A brainstem region that may generate respiratory rhythm in mammals. Science 254, 726-729.
56. Swanson GT, Green T & Heinemann SF (1998). Kainate receptors exhibit differential sensitivities to (S)-5-iodowillardiine. Mol Pharmacol 53, 942-949.
57. Ullah M, Mansor O, Ismail ZI, Kapitonova MY & Sirajudeen KN (2007). Localization of the spinal nucleus of the accessory nerve in rat: A horseradish peroxidase study. J Anat 210, 428-438.
58. Viana F, Bayliss DA & Berger AJ (1993). Calcium conductances and their role in the firing behavior of neonatal rat hypoglossal motoneurons. J Neurophysiol 69, 2137-2149.
59. Wisden W & Seeburg PH (1993). A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13, 3582-3598.
60. Wong LA, Mayer ML, Jane DE & Watkins JC (1994). Willardiines differentiate agonist binding sites for kainate- versus AMPA-preferring glutamate receptors in DRG and hippocampal neurons. J Neurosci 14, 3881-3897.
61. Zeman S & Lodge D (1992). Pharmacological characterization of non-NMDA subtypes of glutamate receptor in the neonatal rat hemisected spinal cord in vitro. Br J Pharmacol 106, 367-372.