Testing the role of preBötzinger complex somatostatin neurons in respiratory and vocal behaviors

European Journal of Neuroscience

Volumn 40, Issue 7, 2014, Pages 3067-3077

  Tupal, Srinivasan ^a   Rieger, Michael A ^a   Ling, Guang Yi ^a   Park, Thomas J ^b   Dougherty, Joseph D ^a   Goodchild, Ann K ^c   Gray, Paul A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

Bat; Naked mole rat; PreB tzinger complex; Respiratory rhythm; Vocalisation

Indexed keywords

GLUTAMIC ACID; MU OPIATE RECEPTOR AGONIST; NEUROKININ 1 RECEPTOR AGONIST; SOMATOSTATIN; VESICULAR GLUTAMATE TRANSPORTER 2; SLC17A6 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BREATHING; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MEDULLA OBLONGATA; MOTONEURON NUCLEUS; MOUSE; NERVE CELL; NONHUMAN; PREBOTZINGER COMPLEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHOMBENCEPHALON; SOMATOSTATIN NEURON; VOCALIZATION; YOUNG ADULT; ANIMAL; BAT; C57BL MOUSE; FEMALE; METABOLISM; MOLE RAT; PHYSIOLOGY; SECRETION (PROCESS); SPECIES DIFFERENCE; TRANSGENIC MOUSE;

ANIMALS; CHIROPTERA; FEMALE; GLUTAMIC ACID; MEDULLA OBLONGATA; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLE RATS; NEURONS; RESPIRATION; SOMATOSTATIN; SPECIES SPECIFICITY; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VOCALIZATION, ANIMAL;

EID: 84908250981     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12669     Document Type: Article

References (91)

1. Alheid, G.F. & McCrimmon, D.R. (2008) The chemical neuroanatomy of breathing. Resp. Physiol. Neurobi., 164, 3-11.
2. Allen, J.P., Hathway, G.J., Clarke, N.J., Jowett, M.I., Topps, S., Kendrick, K.M., Humphrey, P., Wilkinson, L.S. & Emson, P.C. (2003) Somatostatin receptor 2 knockout/lacZ knockin mice show impaired motor coordination and reveal sites of somatostatin action within the striatum. Eur. J. Neurosci., 17, 1881-1895.
3. Andalman, A.S., Foerster, J.N. & Fee, M.S. (2011) Control of vocal and respiratory patterns in birdsong: dissection of forebrain and brainstem mechanisms using temperature. PLoS One, 6, e25461.
4. Arriaga, G., Zhou, E.P. & Jarvis, E.D. (2012) Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds. PLoS One, 7, e46610.
5. Bennett, N.C. & Faulkes, C.G. (2000) African Mole-Rats: Ecology and Eusociality. Cambridge University Press, Cambridge, UK.
6. Bieger, D. & Hopkins, D.A. (1987) Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J. Comp. Neurol., 262, 546-562.
7. Bohn, K.M., Schmidt-French, B., Ma, S.T. & Pollak, G.D. (2008) Syllable acoustics, temporal patterns, and call composition vary with behavioral context in Mexican free-tailed bats. J. Acoust. Soc. Am., 124, 1838-1848.
8. Bouvier, J., Thoby-Brisson, M., Renier, N., Dubreuil, V., Ericson, J., Champagnat, J., Pierani, A., Chedotal, A. & Fortin, G. (2010) Hindbrain interneurons and axon guidance signaling critical for breathing. Nat. Neurosci., 13, 1066-1074.
9. Brett, R.A. (1991) The ecology of naked mole-rat colonies: burrowing, food, and limiting factors. In Sherman, P.W., Jarvis, J.U.M. & Alexander, R.D. (Eds), The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, NJ, pp. 137-184.
10. Burke, P.G., Li, Q., Costin, M.L., McMullan, S., Pilowsky, P.M. & Goodchild, A.K. (2008) Somatostatin 2A receptor-expressing presympathetic neurons in the rostral ventrolateral medulla maintain blood pressure. Hypertension, 52, 1127-1133.
11. Burke, P.G., Abbott, S.B., McMullan, S., Goodchild, A.K. & Pilowsky, P.M. (2010) Somatostatin selectively ablates post-inspiratory activity after injection into the Botzinger complex. Neuroscience, 167, 528-539.
12. Cambronero, F. & Puelles, L. (2000) Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J. Comp. Neurol., 427, 522-545.
13. Carroll, M.S., Viemari, J.-C. & Ramirez, J.-M. (2013) Patterns of inspiratory phase-dependent activity in the in vitro respiratory network. J. Neurophysiol., 109, 285-295.
14. Chiao, G.Z., Larson, C.R., Yajima, Y., Ko, P. & Kahrilas, P.J. (1994) Neuronal activity in nucleus ambiguous during deglutition and vocalisation in conscious monkeys. Experimental brain research. Exp. Brain Res., 100, 29-38.
15. Credner, S., Burda, H. & Ludescher, F. (1997) Acoustic communication underground: vocalisation characteristics in subterranean social mole-rats (Cryptomys sp., Bathyergidae). J. Comp. Physiol. A., 180, 245-255.
16. De Leon, M., Covenas, R., Narrvaez, J., Tramu, G., Aguirre, J. & Gonzalez-Baron, S. (1992) Distribution of somatostatin-28 (1, Äì12) in the cat brainstem: an immunocytochemical study. Neuropeptides, 21, 1-11.
17. Del Negro, C.A., Morgado-Valle, C. & Feldman, J.L. (2002) Respiratory rhythm: an emergent network property? Neuron, 34, 821-830.
18. Doi, A. & Ramirez, J.M. (2010) State-dependent interactions between excitatory neuromodulators in the neuronal control of breathing. J. Neurosci., 30, 8251-8262.
19. Dougherty, J.D., Maloney, S.E., Wozniak, D.F., Rieger, M.A., Sonnenblick, L., Coppola, G., Mahieu, N.G., Zhang, J., Cai, J. & Patti, G.J. (2013) The disruption of Celf6, a gene identified by translational profiling of serotonergic neurons, results in autism-related behaviors. J. Neurosci., 33, 2732-2753.
20. Elliott, W.R. (1993) Air monitoring during construction of a cave gate. Proceedings of the 1993 National Cave Management Symposium, Carlsbad, New Mexico City, pp. 45-51.
21. Feldman, J.L. & Smith, J.C. (1989) Cellular mechanisms underlying modulation of breathing pattern in mammals. Ann. NY Acad. Sci., 563, 114-130.
22. Feldman, J.L., Del Negro, C. & Gray, P.A. (2013) Understanding the rhythm of breathing: so near, yet so far. In Julius, D. & Clapham, D.E. (Eds) Annual Review of Physiology, vol 75. Annual Reviews, Palo Alto, pp. 423-452.
23. Forster, H.V., Krause, K.L., Kiner, T., Neumueller, S.E., Bonis, J.M., Qian, B. & Pan, L.G. (2010) Plasticity of respiratory rhythm-generating mechanisms in adult goats. Adv. Exp. Med. Biol., 669, 151-155.
24. Gourbal, B.E., Barthelemy, M., Petit, G. & Gabrion, C. (2004) Spectrographic analysis of the ultrasonic vocalisations of adult male and female BALB/c mice. Naturwissenschaften, 91, 381-385.
25. Gray, P.A. (2013) Transcription factors define the neuroanatomical organization of the medullary reticular formation. Front. Neuroanat., 7, 7.
26. Gray, P.A., Rekling, J.C., Bocchiaro, C.M. & Feldman, J.L. (1999) Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBotzinger complex. Science, 286, 1566-1568.
27. Gray, P.A., Janczewski, W.A., Mellen, N., McCrimmon, D.R. & Feldman, J.L. (2001) Normal breathing requires preBotzinger complex neurokinin-1 receptor-expressing neurons. Nat. Neurosci., 4, 927-930.
28. Gray, P.A., Hayes, J.A., Ling, G.Y., Llona, I., Tupal, S., Picardo, M.C., Ross, S.E., Hirata, T., Corbin, J.G., Eugenin, J. & Del Negro, C.A. (2010) Developmental origin of preBotzinger complex respiratory neurons. J. Neurosci., 30, 14883-14895.
29. Greer, J.J., Smith, J.C. & Feldman, J.L. (1991) Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J. Physiol., 437, 727-749.
30. Greer, J.J., Smith, J.C. & Feldman, J.L. (1992) Respiratory and locomotor patterns generated in the fetal rat brain stem-spinal cord in vitro. J. Neurophysiol., 67, 996-999.
31. Greer, J.J., Allan, D.W., Martin-Caraballo, M. & Lemke, R.P. (1999) An overview of phrenic nerve and diaphragm muscle development in the perinatal rat. J. Appl. Physiol., 86, 779-786.
32. Hayes, J.A., Wang, X. & Del Negro, C.A. (2012) Cumulative lesioning of respiratory interneurons disrupts and precludes motor rhythms in vitro. Proc. Natl. Acad. Sci. USA, 109, 8286-8291.
33. Heffner, R.S. & Heffner, H.E. (1993) Degenerate hearing and sound localization in naked mole rats (Heterocephalus glaber), with an overview of central auditory structures. J. Comp. Neurol., 331, 418-433.
34. Helke, C. & Hill, K. (1988) Immunohistochemical study of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat. Neuroscience, 26, 539-551.
35. Hodges, M.R., Tattersall, G.J., Harris, M.B., McEvoy, S.D., Richerson, D.N., Deneris, E.S., Johnson, R.L., Chen, Z.F. & Richerson, G.B. (2008) Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J. Neurosci., 28, 2495-2505.
36. Hofer, M.A., Shair, H.N. & Brunelli, S.A. (2002) Ultrasonic vocalisations in rat and mouse pups. Curr. Protoc. Neurosci., 8, 8.14.
37. Holstege, G. (1989) Anatomical study of the final common pathway for vocalisation in the cat. J. Comp. Neurol., 284, 242-252.
38. Holy, T.E. & Guo, Z. (2005) Ultrasonic songs of male mice. PLoS Biol., 3, e386.
39. Hurley, D., Wee, B. & Phelps, C. (1997) Hypophysiotropic somatostatin expression during postnatal development in growth hormone-deficient Ames dwarf mice: mRNA in situ hybridization. Neuroendocrinology, 65, 98-106.
40. Johansson, O., Hokfelt, T. & Elde, R.P. (1984) Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience, 13, 265-339.
41. Jürgens, U. (2009) The neural control of vocalisation in mammals: a review. J. Voice, 23, 1-10.
42. Jurgens, U. & Hage, S.R. (2007) On the role of the reticular formation in vocal pattern generation. Behav. Brain Res., 182, 308-314.
43. Kinkead, R. (2009) Phylogenetic trends in respiratory rhythmogenesis: insights from ectothermic vertebrates. Resp. Physiol. Neurobi., 168, 39-48.
44. Krause, K.L., Forster, H.V., Kiner, T., Davis, S.E., Bonis, J.M., Qian, B. & Pan, L.G. (2009) Normal breathing pattern and arterial blood gases in awake and sleeping goats after near total destruction of the presumed pre-Botzinger complex and the surrounding region. J. Appl. Physiol., 106, 605-619.
45. Lalley, P.M., Pilowsky, P.M., Forster, H.V. & Zuperku, E.J. (2014) CrossTalk opposing view: the pre-Bötzinger complex is not essential for respiratory depression following systemic administration of opioid analgesics. J. Physiol., 592, 1163-1166.
46. Larson, C.R., Yajima, Y. & Ko, P. (1994) Modification in activity of medullary respiratory-related neurons for vocalisation and swallowing. J. Neurophysiol., 71, 2294-2304.
47. Lieske, S.P. & Ramirez, J.M. (2006) Pattern-specific synaptic mechanisms in a multifunctional network. I. Effects of alterations in synapse strength. J. Neurophysiol., 95, 1323-1333.
48. Lieske, S.P., Thoby-Brisson, M., Telgkamp, P. & Ramirez, J.M. (2000) Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps [see comment]. Nat. Neurosci., 3, 600-607.
49. Llona, I. & Eugenin, J. (2005) Central actions of somatostatin in the generation and control of breathing. Biol. Res., 38, 347-352.
50. Llona, I., Ampuero, E. & Eugenin, J.L. (2004) Somatostatin inhibition of fictive respiration is modulated by pH. Brain Res., 1026, 136-142.
51. Low, M.J., Otero-Corchon, V., Parlow, A.F., Ramirez, J.L., Kumar, U., Patel, Y.C. & Rubinstein, M. (2001) Somatostatin is required for masculinization of growth hormone, Äìregulated hepatic gene expression but not of somatic growth. J. Clin. Invest., 107, 1571-1580.
52. Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R., Lein, E.S. & Zeng, H. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci., 13, 133-140.
53. Marin, F., Aroca, P. & Puelles, L. (2008) Hox gene colinear expression in the avian medulla oblongata is correlated with pseudorhombomeric domains. Dev. Biol., 323, 230-247.
54. McKay, L.C. & Feldman, J.L. (2008) Unilateral ablation of pre-Botzinger complex disrupts breathing during sleep but not wakefulness. Am. J. Resp. Crit. Care, 178, 89-95.
55. Mellen, N.M. & Mishra, D. (2010) Functional anatomical evidence for respiratory rhythmogenic function of endogenous bursters in rat medulla. J. Neurosci., 30, 8383-8392.
56. Mellen, N.M. & Thoby-Brisson, M. (2012) Respiratory circuits: development, function and models. Curr. Opin. Neurobiol., 22, 676-685.
57. Mellen, N.M., Janczewski, W.A., Bocchiaro, C.M. & Feldman, J.L. (2003) Opioid-induced quantal slowing reveals dual networks for respiratory rhythm generation. Neuron, 37, 821-826.
58. Montandon, G. & Horner, R. (2014) CrossTalk proposal: the preBötzinger complex is essential for the respiratory depression following systemic administration of opioid analgesics. J. Physiol., 592, 1159-1162.
59. Montandon, G., Qin, W., Liu, H., Ren, J., Greer, J.J. & Horner, R.L. (2011) PreBotzinger complex neurokinin-1 receptor-expressing neurons mediate opioid-induced respiratory depression. J. Neurosci., 31, 1292-1301.
60. Onimaru, H. & Homma, I. (2003) A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J. Neurosci., 23, 1478-1486.
61. Pepper, J.W., Braude, S., Lacey, E. & Sherman, P.W. (1991) Vocalizations of the naked mole-rats. In Sherman, P.W., Jarvis, J.U.M. & Alexander, R.D. (Eds), The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, NJ, pp. 243-274.
62. Pierani, A., Moran-Rivard, L., Sunshine, M.J., Littman, D.R., Goulding, M. & Jessell, T.M. (2001) Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron, 29, 367-384.
63. Portfors, C.V. (2007) Types and functions of ultrasonic vocalisations in laboratory rats and mice. J. Am. Assoc. Lab. Anim., 46, 28-34.
64. Ramírez-Jarquín, J.O., Lara-Hernández, S., Lopez-Guerrero, J.J., Aguileta, M.A., Rivera-Angulo, A.J., Sampieri, A., Vaca, L., Ordaz, B. & Pena-Ortega, F. (2012) Somatostatin modulates generation of inspiratory rhythms and determines asphyxia survival. Peptides, 34, 360-372.
65. Riede, T. (2013) Stereotypic laryngeal and respiratory motor patterns generate different call types in rat ultrasound vocalisation. J. Exp. Zool. Part A., 319, 213-224.
66. Rossi, J., Balthasar, N., Olson, D., Scott, M., Berglund, E., Lee, C.E., Choi, M.J., Lauzon, D., Lowell, B.B. & Elmquist, J.K. (2011) Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab., 13, 195-204.
67. Ruangkittisakul, A., Schwarzacher, S.W., Secchia, L., Ma, Y., Bobocea, N., Poon, B.Y., Funk, G.D. & Ballanyi, K. (2008) Generation of eupnea and sighs by a spatiochemically organized inspiratory network. J. Neurosci., 28, 2447-2458.
68. Rubsamen, R. (1987) Ontogenesis of the echolocation system in the rufous horseshoe bat, Rhinolophus rouxi (audition and vocalisation in early postnatal development). J. Comp. Physiol. A., 161, 899-913.
69. Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 9, 671-675.
70. Smith, J.C., Ellenberger, H.H., Ballanyi, K., Richter, D.W. & Feldman, J.L. (1991) Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science, 254, 726-729.
71. Smotherman, M.S. (2007) Sensory feedback control of mammalian vocalisations. Behav. Brain Res., 182, 315-326.
72. Stornetta, R.L., Rosin, D.L., Wang, H., Sevigny, C.P., Weston, M.C. & Guyenet, P.G. (2003) A group of glutamatergic interneurons expressing high levels of both neurokinin-1 receptors and somatostatin identifies the region of the pre-Botzinger complex. J. Comp. Neurol., 455, 499-512.
73. Taber-Pierce, E., Lichentenstein, E. & Feldman, S.C. (1985) The somatostatin systems of the guinea-pig brainstem. Neuroscience, 15, 215-235.
74. Tachibana, M., Rothman, J.M. & Guth, P.S. (1979) Somatostatin along the auditory pathway. Hearing Res., 1, 365-368.
75. Tan, W., Janczewski, W.A., Yang, P., Shao, X.M., Callaway, E.M. & Feldman, J.L. (2008) Silencing preBotzinger Complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nat. Neurosci., 11, 538-540.
76. Tanaka, D.H., Oiwa, R., Sasaki, E. & Nakajima, K. (2011) Changes in cortical interneuron migration contribute to the evolution of the neocortex. Proc. Natl. Acad. Sci. USA, 108, 8015-8020.
77. Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsiani, D., Fu, Y., Lu, J., Lin, Y., Miyoshi, G., Shima, Y., Fishell, G., Nelson, S.B. & Huang, Z.J. (2011) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron, 71, 995-1013.
78. Telgkamp, P., Cao, Y.Q., Basbaum, A.I. & Ramirez, J.M. (2002) Long-term deprivation of substance P in PPT-A mutant mice alters the anoxic response of the isolated respiratory network. J. Neurophysiol., 88, 206-213.
79. Thoby-Brisson, M., Trinh, J.B., Champagnat, J. & Fortin, G. (2005) Emergence of the pre-Botzinger respiratory rhythm generator in the mouse embryo. J. Neurosci., 25, 4307-4318.
80. Tong, Q., Ye, C., McCrimmon, R.J., Dhillon, H., Choi, B., Kramer, M.D., Yu, J., Yang, Z., Christiansen, L.M., Lee, C.E., Choi, C.S., Zigman, J.M., Shulman, G.I., Sherwin, R.S., Elmquist, J.K. & Lowell, B.B. (2007) Synaptic glutamate release by ventromedial hypothalamic neurons is part of the neurocircuitry that prevents hypoglycemia. Cell Metab., 5, 383-393.
81. Tupal, S., Huang, W.H., Picardo, M.C., Ling, G.Y., Del Negro, C., Zoghbi, H.Y. & Gray, P.A. (2014) Atoh1-dependent rhombic lip neurons are required for temporal delay between independent respiratory oscillators in embryonic mice. eLife, 3, e02265.
82. Van Daele, D.J. & Cassell, M.D. (2009) Multiple forebrain systems converge on motor neurons innervating the thyroarytenoid muscle. Neuroscience, 162, 501-524.
83. Van Daele, D.J., Fazan, V.P., Agassandian, K. & Cassell, M.D. (2011) Amygdala connections with jaw, tongue and laryngo-pharyngeal premotor neurons. Neuroscience, 177, 93-113.
84. Wallen-Mackenzie, A., Gezelius, H., Thoby-Brisson, M., Nygard, A., Enjin, A., Fujiyama, F., Fortin, G. & Kullander, K. (2006) Vesicular glutamate transporter 2 is required for central respiratory rhythm generation but not for locomotor central pattern generation. J. Neurosci., 26, 12294-12307.
85. Wallen-Mackenzie, A., Wootz, H. & Englund, H. (2010) Genetic inactivation of the vesicular glutamate transporter 2 (VGLUT2) in the mouse: what have we learnt about functional glutamatergic neurotransmission? Upsala J. Med. Sci., 115, 11-20.
86. Wang, X., Hayes, J.A., Picardo, M.C. & Del Negro, C.A. (2013) Automated cell-specific laser detection and ablation of neural circuits in neonatal brain tissue. J. Physiol., 591, 2393-2401.
87. Wenninger, J.M., Pan, L.G., Klum, L., Leekley, T., Bastastic, J., Hodges, M.R., Feroah, T., Davis, S. & Forster, H.V. (2004a) Small reduction of neurokinin-1 receptor-expressing neurons in the pre-Botzinger complex area induces abnormal breathing periods in awake goats. J. Appl. Physiol., 97, 1620-1628.
88. Wenninger, J.M., Pan, L.G., Klum, L., Leekley, T., Bastastic, J., Hodges, M.R., Feroah, T.R., Davis, S. & Forster, H.V. (2004b) Large lesions in the pre-Botzinger complex area eliminate eupneic respiratory rhythm in awake goats. J. Appl. Physiol., 97, 1629-1636.
89. Wild, J., Goller, F. & Suthers, R. (1998) Inspiratory muscle activity during bird song. J. Neurobiol., 36, 441-453.
90. Wonders, C.P. & Anderson, S.A. (2006) The origin and specification of cortical interneurons. Nat. Rev. Neurosci., 7, 687-696.
91. Yosida, S., Kobayasi, K.I., Ikebuchi, M., Ozaki, R. & Okanoya, K. (2007) Antiphonal Vocalization of a Subterranean Rodent, the Naked Mole Rat (Heterocephalus glaber). Ethology, 113, 703-710.