Selective optogenetic activation of rostral ventrolateral medullary catecholaminergic neurons produces cardiorespiratory stimulation in conscious mice

Journal of Neuroscience

Volumn 33, Issue 7, 2013, Pages 3164-3177

  Abbott, Stephen B G ^a   DePuy, Seth D ^a   Nguyen, Thanh ^a   Coates, Melissa B ^a   Stornetta, Ruth L ^a   Guyenet, Patrice G ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAMINOBENZIDINE; VESICULAR GLUTAMATE TRANSPORTER 2;

ANESTHESIA INDUCTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; BRADYCARDIA; BREATHING RATE; CATECHOLAMINERGIC SYSTEM; CELL ACTIVATION; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; ELECTROMYOGRAPHY; FEMALE; HISTOLOGY; HYPERCAPNIA; HYPOTENSION; HYPOXIA; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; OPTOGENETICS; PHOTOSTIMULATION; PRIORITY JOURNAL; RESPIRATORY FUNCTION; THALAMUS VENTRAL NUCLEUS;

ANIMALS; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; CATECHOLAMINES; CEREBROVASCULAR CIRCULATION; CONSCIOUSNESS; DEPENDOVIRUS; DOPAMINE BETA-HYDROXYLASE; FEMALE; GENETIC VECTORS; HYPERCAPNIA; HYPEROXIA; IMMUNOHISTOCHEMISTRY; LUMINESCENT PROTEINS; MALE; MEDULLA OBLONGATA; MICE; MICROINJECTIONS; NEURONS; PHOTIC STIMULATION; RESPIRATORY PHYSIOLOGICAL PHENOMENA; RHODOPSIN;

EID: 84873654803     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1046-12.2013     Document Type: Article

References (71)

1. Abbott SB, Stornetta RL, Fortuna MG, Depuy SD, West GH, Harris TE, Guyenet PG (2009a) Photostimulation of retrotrapezoid nucleus phox2b-expressing neurons in vivo produces long-lasting activation of breathing in rats. J Neurosci 29:5806-5819. CrossRef Medline
2. Abbott SB, Stornetta RL, Socolovsky CS, West GH, Guyenet PG (2009b) Photostimulation of channelrhodopsin-2 expressing ventrolateral medullary neurons increases sympathetic nerve activity and blood pressure in rats. J Physiol 587:5613-5631. CrossRef Medline
3. Abbott SB, Stornetta RL, Coates MB, Guyenet PG (2011) Phox2b-expressing neurons of the parafacial region regulate breathing rate, inspiration, and expiration in conscious rats. J Neurosci 31:16410-16422. CrossRef Medline
4. Aicher SA, Saravay RH, Cravo S, Jeske I, Morrison SF, Reis DJ, Milner TA (1996) Monosynaptic projections from the nucleus tractus solitarii to C1 adrenergic neurons in the rostral ventrolateral medulla: comparison with input from the caudal ventrolateral medulla. J Comp Neurol 373:62-75. CrossRef Medline
5. Arango V, Ruggiero DA, Callaway JL, Anwar M, Mann JJ, Reis DJ (1988) Catecholaminergic neurons in the ventrolateral medulla and nucleus of the solitary tract in the human. J Comp Neurol 273:224-240. CrossRef Medline
6. Aston-Jones G, Chen S, Zhu Y, Oshinsky ML (2001) A neural circuit for circadian regulation of arousal. Nat Neurosci 4:732-738. CrossRef Medline
7. Ballanyi K (2004) Protective role of neuronal KATP channels in brain hypoxia. J Exp Biol 207:3201-3212. CrossRef Medline
8. Ben-Tal A, Shamailov SS, Paton JF (2012) Evaluating the physiological significance of respiratory sinus arrhythmia: looking beyond ventilation-perfusion efficiency. J Physiol 590:1989-2008. CrossRef Medline
9. Biancardi V, Bícego KC, Almeida MC, Gargaglioni LH (2008) Locus coeruleus noradrenergic neurons and CO2 drive to breathing. Pflugers Arch 455:1119-1128. CrossRef Medline
10. Brown DL, Guyenet PG (1985) Electrophysiological study of cardiovascular neurons in the rostral ventrolateral medulla in rats. Circ Res 56:359-369. CrossRef Medline
11. Butz GM, Davisson RL (2001) Long-term telemetric measurement of cardiovascular parameters in awake mice: a physiological genomics tool. Physiol Genomics 5:89-97. Medline
12. Cao WH, Morrison SF (2001) Differential chemoreceptor reflex responses of adrenal preganglionic neurons. Am J Physiol Regul Integr Comp Physiol 281:R1825-R1832. Medline
13. Card JP, Sved JC, Craig B, Raizada M, Vazquez J, Sved AF (2006) Efferent projections of rat rostroventrolateral medulla C1 catecholamine neurons: implications for the central control of cardiovascular regulation. J Comp Neurol 499:840-859. CrossRef Medline
14. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663-667. CrossRef Medline
15. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2010) Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat Protoc 5:247-254. CrossRef Medline
16. Chamberlin NL (2004) Functional organization of the parabrachial complex and intertrigeminal region in the control of breathing. Respir Physiol Neurobiol 143:115-125. CrossRef Medline
17. Chamberlin NL, Saper CB (1992) Topographic organization of cardiovascular responses to electrical and glutamate microstimulation of the parabrachial nucleus in the rat. J Comp Neurol 326:245-262. CrossRef Medline
18. Chitravanshi VC, Sapru HN (1995) Chemoreceptor-sensitive neurons in commissural subnucleus of nucleus tractus solitarius of the rat. Am J Physiol 268:R851-R858. Medline
19. Depuy SD, Kanbar R, Coates MB, Stornetta RL, Guyenet PG (2011) Control of breathing by raphe obscurus serotonergic neurons in mice. J Neurosci 31:1981-1990. CrossRef Medline
20. Depuy SD, Stornetta RL, Bochorishvili G, Deisseroth K, Witten I, Coates MB, Guyenet PG (2013) Glutamatergic neurotransmission between the C1 neurons and the parasympathetic preganglionic neurons of the dorsal motor nucleus of the vagus. J Neurosci. 33:1486-1497. CrossRef Medline
21. DiMicco JA, Samuels BC, Zaretskaia MV, Zaretsky DV (2002) The dorsomedial hypothalamus and the response to stress: part renaissance, part revolution. Pharmacol Biochem Behav 71:469-480. CrossRef Medline
22. Dormer KJ, Anwar M, Ashlock SR, Ruggiero DA (1993) Organization of presumptive catecholamine-synthesizing neurons in the canine medullaoblongata. Brain Res 601:41-64. CrossRef Medline
23. Drorbaugh JE, Fenn WO (1955) A barometric method for measuring ventilation in newborn infants. Pediatrics 16:81-87. Medline
24. Erickson JT, Millhorn DE (1994) Hypoxia and electrical stimulation of the carotid sinus nerve induce c-Fos-like immunoreactivity within catecholaminergic and serotinergic neurons of the rat brainstem. J Comp Neurol 348:161-182. CrossRef Medline
25. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260. CrossRef Medline
26. Funk GD, Huxtable AG, Lorier AR (2008) ATP in central respiratory control: a three-part signaling system. Respir Physiol Neurobiol 164:131-142. CrossRef Medline
27. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925. CrossRef Medline
28. Guyenet PG (2006) The sympathetic control of blood pressure. Nat Rev Neurosci 7:335-346. CrossRef Medline
29. Guyenet PG, Stornetta RL, Bayliss DA (2010) Central respiratory chemoreception. J Comp Neurol 518:3883-3906. CrossRef Medline
30. Hayano J, Yasuma F, Okada A, Mukai S, Fujinami T (1996) Respiratory sinus arrhythmia. A phenomenon improving pulmonary gas exchange and circulatory efficiency. Circulation 94:842-847. CrossRef Medline
31. Hirooka Y, Polson JW, Potts PD, Dampney RA (1997) Hypoxia-induced Fos expression in neurons projecting to the pressor region in the rostral ventrolateral medulla. Neuroscience 80:1209-1224. CrossRef Medline
32. Hodges MR, Richerson GB (2010) The role of medullary serotonin (5-HT) neurons in respiratory control: contributions to eupneic ventilation, CO2 chemoreception, and thermoregulation. J Appl Physiol 108:1425-1432. CrossRef Medline
33. Hodges MR, Tattersall GJ, Harris MB, McEvoy SD, Richerson DN, Deneris ES, Johnson RL, Chen ZF, Richerson GB (2008) Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J Neurosci 28:2495-2505. CrossRef Medline
34. Hokfelt T, Fuxe K, Goldstein M, Johansson O (1974) Immunohistochemical evidence for the existence of adrenaline neurons in the rat brain. Brain Res 66:235-251. CrossRef
35. Kang BJ, Chang DA, Mackay DD, West GH, Moreira TS, Takakura AC, Gwilt JM, Guyenet PG, Stornetta RL (2007) Central nervous system distribution of the transcription factor Phox2b in the adult rat. J Comp Neurol 503:627-641. CrossRef Medline
36. Koizumi K, Terui N, Kollai M, Brooks CM (1982) Functional significance of coactivation of vagal and sympathetic cardiac nerves. Proc Natl Acad Sci USA 79:2116-2120. CrossRefMedline
37. Koizumi K, Terui N, Kollai M (1983) Neural control of the heart: significance of double innervation re-examined. J Auton Nerv Syst 7:279-294. CrossRef Medline
38. Kollai M, Koizumi K, Brooks CM (1978) Nature of differential sympathetic discharges in chemoreceptor reflexes. Proc Natl Acad Sci U S A 75:5239-5243 [LIBR]. CrossRef Medline
39. Kubin L, Alheid GF, Zuperku EJ, McCrimmon DR (2006) Central pathways of pulmonary and lower airway vagal afferents. J Appl Physiol 101:618-627. CrossRef Medline
40. Kuwaki T (2010) Hypothalamic modulation of breathing. Adv Exp Med Biol 669:243-247. CrossRef Medline
41. Lazarenko RM, Milner TA, Depuy SD, Stornetta RL, West GH, Kievits JA, Bayliss DA, Guyenet PG (2009) Acid sensitivity and ultrastructure of the retrotrapezoid nucleus in Phox2b-EGFP transgenic mice. J Comp Neurol 517:69-86. CrossRef Medline
42. Li A, Nattie E (2010) Antagonism of rat orexin receptors by almorexant attenuates central chemoreception in wakefulness in the active period of the diurnal cycle. J Physiol 588:2935-2944. CrossRef Medline
43. Li AJ, Wang Q, Dinh TT, Ritter S (2009) Simultaneous silencing of Npy and Dbh expression in hindbrain A1/C1 catecholamine cells suppresses glucoprivic feeding. J Neurosci 29:280-287. CrossRef Medline
44. Li S, Kirouac GJ (2012) Sources of inputs to the anterior and posterior aspects of the paraventricular nucleus of the thalamus. Brain Struct Funct 217:257-273. CrossRef Medline
45. Lipski J, Kanjhan R, Kruszewska B, Smith M (1995) Barosensitive neurons in the rostral ventrolateral medulla of the rat in vivo: morphological properties and relationship to C1 adrenergic neurons. Neuroscience 69:601-618. CrossRef Medline
46. Marina N, Abdala AP, Trapp S, Li A, Nattie EE, Hewinson J, Smith JC, Paton JF, Gourine AV (2010) Essential role of Phox2b-expressing ventrolateral brainstem neurons in the chemosensory control of inspiration and expiration. J Neurosci 30:12466-12473. CrossRef Medline
47. Marina N, Abdala AP, Korsak A, Simms AE, Allen AM, Paton JF, Gourine AV (2011) Control of sympathetic vasomotor tone by catecholaminergic C1 neurones of the rostral ventrolateral medulla oblongata. Cardiovasc Res 91:703-710. CrossRef Medline
48. McAllen RM, May CN, Shafton AD (1995) Functional anatomy of sympathetic premotor cell groups in the medulla. Clin Exp Hypertens 17:209-221. CrossRef Medline
49. McMullan S, Pilowsky PM (2010) The effects of baroreceptor stimulation on central respiratory drive: a review. Respir Physiol Neurobiol 174:37-42. CrossRef Medline
50. Moreira TS, Takakura AC, Colombari E, Guyenet PG (2006) Central chemoreceptors and sympathetic vasomotor outflow. J Physiol 577: 369-386. CrossRef Medline
51. Nattie E, Li A (2010) Central chemoreception in wakefulness and sleep: evidence for a distributed network and a role for orexin. J Appl Physiol 108:1417-1424. CrossRef Medline
52. Paton JF, Boscan P, Pickering AE, Nalivaiko E (2005) The yin and yang of cardiac autonomic control: vago-sympathetic interactions revisited. Brain Res Brain Res Rev 49:555-565. Medline
53. Pilowsky PM, Jiang C, Lipski J (1990) An intracellular study of respiratory neurons in the rostral ventrolateral medulla of the rat and their relationship to catecholamine-containing neurons. J Comp Neurol 301:604-617. CrossRef Medline
54. Potts JT, Rybak IA, Paton JF (2005) Respiratory rhythm entrainment by somatic afferent stimulation. J Neurosci 25:1965-1978. CrossRef Medline
55. Reiner PB, Vincent SR (1986) The distribution of tyrosine hydroxylase, dopamine-B-hydroxylase, and phenylethanolamine-N-methyltransferase immunoreactive neurons in the feline medulla oblongata. J Comp Neurol 248: 518-531. CrossRef Medline
56. Ritter S, Llewellyn-Smith I, Dinh TT (1998) Subgroups of hindbrain catecholamine neurons are selectively activated by 2-deoxy-D-glucose induced metabolic challenge. Brain Res 805:41-54. CrossRef Medline
57. Ruggiero DA, Anwar M, Gootman PM (1992) Presumptive adrenergic neurons containing phenylethanolamine N-methyltransferase immunoreactivity in the medulla oblongata of neonatal swine. Brain Res 583:105-119. CrossRef Medline
58. Sapru HN (1996) Carotid chemoreflex. Neural pathways and transmitters. Adv Exp Med Biol 410:357-364. CrossRef Medline
59. Schiltz JC, Sawchenko PE (2007) Specificity and generality of the involvement of catecholaminergic afferents in hypothalamic responses to immune insults. J Comp Neurol 502:455-467. CrossRef Medline
60. Schreihofer AM, Guyenet PG (1997) Identification of C1 presympathetic neurons in rat rostral ventrolateral medulla by juxtacellular labeling in vivo. J Comp Neurol 387:524-536. CrossRef Medline
61. Sparta DR, Stamatakis AM, Phillips JL, Hovels ø N, van Zessen R, Stuber GD (2012) Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat Protoc 7:12-23. CrossRef Medline
62. Spyer KM, Gourine AV (2009) Chemosensory pathways in the brainstem controlling cardiorespiratory activity. Philos Trans R Soc Lond B Biol Sci 364:2603-2610. CrossRef Medline
63. Stornetta RL, Sevigny CP, Guyenet PG (2002) Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J Comp Neurol 444:191-206. CrossRef Medline
64. Stornetta RL, Macon CJ, Nguyen TM, Coates MB, Guyenet PG (2012) Cholinergic neurons in the mouse rostral ventrolateral medulla target sensory afferent areas. Brain Struct Funct. Advance online publication. doi: 10.1007/s00429-012-0408-3. CrossRef Medline
65. Sun MK (1996) Pharmacology of reticulospinal vasomotor neurons in cardiovascular regulation. Pharm Rev 48:465-494. Medline
66. Sun MK, Reis DJ (1996) Medullary vasomotor activity and hypoxic sympathoexcitation in pentobarbital-anesthetized rats. Am J Physiol 270: R348-R355. Medline
67. Sun MK, Spyer KM (1991a) Nociceptive inputs into rostral ventrolateral medulla spinal vasomotor neurones in rats. J Physiol 436:685-700. Medline
68. Sun MK, Spyer KM (1991b) Responses of rostroventrolateral medulla spinal vasomotor neurones to chemoreceptor stimulation in rats. J Auton Nerv Syst 33:79-84. CrossRef Medline
69. Teppema LJ, Veening JG, Kranenburg A, Dahan A, Berkenbosch A, Olievier C (1997) Expression of c-fos in the rat brainstem after exposure to hypoxia and to normoxic and hyperoxic hypercapnia. J Comp Neurol 388:169-190. CrossRef Medline
70. Vimercati C, Qanud K, Ilsar I, Mitacchione G, Sarnari R, Mania D, Faulk R, Stanley WC, Sabbah HN, Recchia FA (2012) Acute vagal stimulation attenuates cardiac metabolic response to beta-adrenergic stress. J Physiol 590:6065-6074. CrossRef Medline
71. Zanella S, Roux JC, Viemari JC, Hilaire G (2006) Possible modulation of the mouse respiratory rhythm generator by A1/C1 neurones. Respir Physiol Neurobiol 153:126-138. CrossRef Medline