Multiscale fingerprinting of neuronal functional connectivity

Brain Structure and Function

Volumn 220, Issue 5, 2015, Pages 2967-2982

  Song, Gang ^a   Tin, Chung ^a,b   Poon, Chi Sang ^a  

^a Massachusetts Institute of Technology   (United States)

^b CITY UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Functional connectivity; K lliker Fuse nucleus; Laryngeal motoneurons; Multiscale fingerprinting; Pneumotaxic center; Pons; Post inspiratory activity; Respiratory rhythm

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; CELL MARKER;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL PRESSURE; ARTICLE; BREATHING; BREATHING MECHANICS; CENTRAL PATTERN GENERATOR; CHEMORECEPTOR; CONNECTOME; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; HYPOXIA; IMMUNOHISTOLOGY; INTERNEURON; LATERAL RETICULAR NUCLEUS; MAMMAL; MOTONEURON; MOTOR ACTIVITY; NERVE CELL; NEUROMODULATION; NEURONAL FUNCTIONAL CONNECTIVITY; NEUROSCIENCE; NONHUMAN; PARABRACHIAL NUCLEUS; PHASE TRANSITION; PRIORITY JOURNAL; RAT; SUPERIOR CEREBELLAR PEDUNCLE; TRIGEMINAL MOTOR NUCLEUS; ACTION POTENTIAL; ANIMAL; MEDULLA OBLONGATA; NERVE CELL NETWORK; NERVE TRACT; PHYSIOLOGY; PONS;

ACTION POTENTIALS; ANIMALS; MEDULLA OBLONGATA; NERVE NET; NEURAL PATHWAYS; NEURONS; PONS; RATS;

EID: 84940600478     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0838-1     Document Type: Article

References (61)

1. Abbott A (2013) Solving the brain. Nature 499(7458):272–274
2. Alivisatos AP, Chun M, Church GM, Greenspan RJ, Roukes ML, Yuste R (2012) The brain activity map project and the challenge of functional connectomics. Neuron 74(6):970–974. doi:10.1016/j.neuron.2012.06.006
3. Alivisatos AP, Andrews AM, Boyden ES, Chun M, Church GM, Deisseroth K, Donoghue JP, Fraser SE, Lippincott-Schwartz J, Looger LL, Masmanidis S, McEuen PL, Nurmikko AV, Park H, Peterka DS, Reid C, Roukes ML, Scherer A, Schnitzer M, Sejnowski TJ, Shepard KL, Tsao D, Turrigiano G, Weiss PS, Xu C, Yuste R, Zhuang X (2013) Nanotools for neuroscience and brain activity mapping. ACS Nano 7(3):1850–1866. doi:10.1021/nn4012847
4. Bautista TG, Dutschmann M (2014) Ponto-medullary nuclei involved in the generation of sequential pharyngeal swallowing and concomitant protective laryngeal adduction in situ. J Physiol. doi:10.1113/jphysiol.2014.272468
5. Cohen MI, Wang SC (1959) Respiratory neuronal activity in pons of cat. J Neurophysiol 22(1):33–50
6. de la Rocha J, Doiron B, Shea-Brown E, Josic K, Reyes A (2007) Correlation between neural spike trains increases with firing rate. Nature 448(7155):802–806. doi:10.1038/nature06028
7. Devor A, Bandettini PA, Boas DA, Bower JM, Buxton RB, Cohen LB, Dale AM, Einevoll GT, Fox PT, Franceschini MA, Friston KJ, Fujimoto JG, Geyer MA, Greenberg JH, Halgren E, Hamalainen MS, Helmchen F, Hyman BT, Jasanoff A, Jernigan TL, Judd LL, Kim SG, Kleinfeld D, Kopell NJ, Kutas M, Kwong KK, Larkum ME, Lo EH, Magistretti PJ, Mandeville JB, Masliah E, Mitra PP, Mobley WC, Moskowitz MA, Nimmerjahn A, Reynolds JH, Rosen BR, Salzberg BM, Schaffer CB, Silva GA, So PT, Spitzer NC, Tootell RB, Van Essen DC, Vanduffel W, Vinogradov SA, Wald LL, Wang LV, Weber B, Yodh AG (2013) The challenge of connecting the dots in the B.R.A.I.N. Neuron 80(2):270–274. doi:10.1016/j.neuron.2013.09.008
8. Dick TE, Bellingham MC, Richter DW (1994) Pontine respiratory neurons in anesthetized cats. Brain Res 636(2):259–269
9. Dutschmann M, Dick TE (2012) Pontine mechanisms of respiratory control. Compr Physiol 2(4):2443–2469. doi:10.1002/cphy.c100015
10. Dutschmann M, Herbert H (2006) The Kolliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. Eur J Neurosci 24(4):1071–1084
11. Dutschmann M, Menuet C, Stettner GM, Gestreau C, Borghgraef P, Devijver H, Gielis L, Hilaire G, Van Leuven F (2010) Upper airway dysfunction of Tau-P301L mice correlates with tauopathy in midbrain and ponto-medullary brainstem nuclei. J Neurosci 30(5):1810–1821. doi:10.1523/JNEUROSCI.5261-09.2010
12. Ezure K, Tanaka I (2006) Distribution and medullary projection of respiratory neurons in the dorsolateral pons of the rat. Neuroscience 141(2):1011–1023. doi:10.1016/j.neuroscience.2006.04.020
13. Ezure K, Tanaka I, Kondo M (2003) Glycine is used as a transmitter by decrementing expiratory neurons of the ventrolateral medulla in the rat. J Neurosci 23(26):8941–8948
14. Hampson-Evans D, Morgan P, Farrar M (2008) Pediatric laryngospasm. Paediatr Anaesth 18(4):303–307. doi:10.1111/j.1460-9592.2008.02446.x
15. Helmstaedter M (2013) Cellular-resolution connectomics: challenges of dense neural circuit reconstruction. Nat Methods 10(6):501–507. doi:10.1038/nmeth.2476
16. Hempel CM, Sugino K, Nelson SB (2002) Multi-unit spike-triggered averaging: a method for probing the physiology of central synapses. J Neurosci Methods 120(2):121–129
17. Hoh JFY (2010) Laryngeal muscles as highly specialized organs in airway protection, respiration and phonation. Hbk Behav Neurosci 19:13–21. doi:10.1016/B978-0-12-374593-4.00002-4
18. Kirkwood PA (1979) On the use and interpretation of cross-correlations measurements in the mammalian central nervous system. J Neurosci Methods 1(2):107–132
19. 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(1):60–68
20. Lindsey BG, Rybak IA, Smith JC (2012) Computational models and emergent properties of respiratory neural networks. Compr Physiol 2(3):1619–1670. doi:10.1002/cphy.c110016
21. Ludlow CL (2011) Central nervous system control of interactions between vocalization and respiration in mammals. Head Neck 33(Suppl 1):S21–S25. doi:10.1002/hed.21904
22. Lumsden T (1923) Observations on the respiratory centres in the cat. J Physiol London 57:153–160
23. MacDonald SM, Tin C, Song G, Poon CS (2009) Use-dependent learning and memory of the Hering-Breuer inflation reflex in rats. Exp Physiol 94(2):269–278. doi:10.1113/expphysiol.2008.045344
24. Maltby A, Jones KE, Jones G (2010) Understanding the evolutionary origin and diversification of bat echolocation calls. Hbk Behav Neurosci 19:37–47. doi:10.1016/B978-0-12-374593-4.0005-X
25. Martin RJ, Wilson CG (2012) Apnea of prematurity. Compr Physiol 2(4):2923–2931. doi:10.1002/cphy.c100021
26. Molkov YI, Bacak BJ, Dick TE, Rybak IA (2013) Control of breathing by interacting pontine and pulmonary feedback loops. Front Neural Circuits 7:16. doi:10.3389/fncir.2013.00016
27. Ostojic S, Brunel N, Hakim V (2009) How connectivity, background activity, and synaptic properties shape the cross-correlation between spike trains. J Neurosci 29(33):10234–10253. doi:10.1523/JNEUROSCI.1275-09.2009
28. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, San Diego
29. Paxinos G, Carrive P, Wang H, Wang P (1999) Chemo architectonic atlas of the rat brainstem. Academic Press, San Diego
30. Pernice V, Staude B, Cardanobile S, Rotter S (2011) How structure determines correlations in neuronal networks. PLoS Comput Biol 7(5):e1002059. doi:10.1371/journal.pcbi.1002059
31. Pitts T (2013) Airway protective mechanisms. Lung. doi:10.1007/s00408-013-9540-y
32. Poon CS, Song G (2014) Bidirectional plasticity of pontine pneumotaxic postinspiratory drive: implication for a pontomedullary respiratory central pattern generator. Prog Brain Res 209:235–254. doi:10.1016/B978-0-444-63274-6.00012-6
33. Richter DW, Ballanyi K, Schwarzacher S (1992) Mechanisms of respiratory rhythm generation. Curr Opin Neurobiol 2(6):788–793
34. Segers LS, Shannon R, Lindsey BG (1985) Interactions between rostral pontine and ventral medullary respiratory neurons. J Neurophysiol 54(2):318–334
35. Segers LS, Nuding SC, Dick TE, Shannon R, Baekey DM, Solomon IC, Morris KF, Lindsey BG (2008) Functional connectivity in the pontomedullary respiratory network. J Neurophysiol 100(4):1749–1769. doi:10.1152/jn.90414.2008
36. Shevtsova NA, Manzke T, Molkov YI, Bischoff A, Smith JC, Rybak IA, Richter DW (2011) Computational modelling of 5-HT receptor-mediated reorganization of the brainstem respiratory network. Eur J Neurosci 34(8):1276–1291. doi:10.1111/j.1460-9568.2011.07825.x
37. Shiba K (2010) Functions of larynx in breathing, vocalization and airway protective reflexes. In: Brudzynski SM (ed) Handbook of mammalian vocalization: an integrative neuroscience approach, vol 19., Handbook of behavioral neuroscienceElsevier Science Bv, Amsterdam, pp 373–381. doi:10.1016/b978-0-12-374593-4.00034-6
38. Siniaia MS, Young DL, Poon CS (2000) Habituation and desensitization of the Hering-Breuer reflex in rat. J Physiol 523(Pt 2):479–491
39. Smith JC, Abdala AP, Koizumi H, Rybak IA, Paton JF (2007) Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms. J Neurophysiol 98(6):3370–3387
40. Smith JC, Abdala AP, Borgmann A, Rybak IA, Paton JF (2013) Brainstem respiratory networks: building blocks and microcircuits. Trends Neurosci 36(3):152–162. doi:10.1016/j.tins.2012.11.004
41. Smotherman M, Zhang S, Metzner W (2003) A neural basis for auditory feedback control of vocal pitch. J Neurosci 23(4):1464–1477
42. Smotherman M, Kobayasi K, Ma J, Zhang S, Metzner W (2006) A mechanism for vocal-respiratory coupling in the mammalian parabrachial nucleus. J Neurosci 26(18):4860–4869. doi:10.1523/JNEUROSCI.4607-05.2006
43. Smotherman M, Schwartz C, Metzner W (2010) Vocal-respiratory interactions in the parabrachial nucleus. In: Brudzynski SM (ed) Handbook of Mammalian Vocalization: An Integrative Neuroscience Approach, vol 19., Handbook of Behavioral NeuroscienceElsevier Science Bv, Amsterdam, pp 383–392. doi:10.1016/b978-0-12-374593-4.00035-8
44. Song G, Poon C (2009) Lateral parabrachial nucleus mediates shortening of expiration during hypoxia. Respir Physiol Neurobiol 165(1):1–8
45. Song G, Yu Y, Poon CS (2006) Cytoarchitecture of pneumotaxic integration of respiratory and nonrespiratory information in the rat. J Neurosci 26(1):300–310. doi:10.1523/JNEUROSCI.3029-05.2006
46. +/− mutant mouse model of Rett Syndrome. Front Integr Neurosci 5:6. doi:10.3389/fnint.2011.00006
47. Song G, Xu H, Wang H, Macdonald SM, Poon C-S (2011b) Hypoxia-excited neurons in NTS send axonal projections to Kolliker-Fuse/parabrachial complex in dorsolateral pons. Neuroscience 175:145–153. doi:10.1016/j.neuroscience.2010.11.065
48. Song G, Wang H, Xu H, Poon CS (2012) Kolliker-Fuse neurons send collateral projections to multiple hypoxia-activated and nonactivated structures in rat brainstem and spinal cord. Brain Struct Funct 217(4):835–858. doi:10.1007/s00429-012-0384-7
49. Stettner GM, Huppke P, Brendel C, Richter DW, Gartner J, Dutschmann M (2007) Breathing dysfunctions associated with impaired control of postinspiratory activity in Mecp2-/y knockout mice. J Physiol 579(Pt 3):863–876
50. Stettner GM, Zanella S, Huppke P, Gartner J, Hilaire G, Dutschmann M (2008) Spontaneous central apneas occur in the C57BL/6 J mouse strain. Respir Physiol Neurobiol 160(1):21–27. doi:10.1016/j.resp.2007.07.011
51. Subramanian HH (2013) Descending control of the respiratory neuronal network by the midbrain periaqueductal grey in the rat in vivo. J Physiol 591(Pt 1):109–122. doi:10.1113/jphysiol.2012.245217
52. te Pas AB, Wong C, Kamlin CO, Dawson JA, Morley CJ, Davis PG (2009) Breathing patterns in preterm and term infants immediately after birth. Pediatr Res 65(3):352–356. doi:10.1203/PDR.0b013e318193f117
53. Trousdale J, Hu Y, Shea-Brown E, Josic K (2012) Impact of network structure and cellular response on spike time correlations. PLoS Comput Biol 8(3):e1002408. doi:10.1371/journal.pcbi.1002408
54. von Euler C (1977) The functional organization of the respiratory phase-switching mechanisms. Fed Proc 36(10):2375–2380
55. Wang H, Zhang H, Song G, Poon CS (2008) Modulation of Hering-Breuer reflex by ventrolateral pons. Adv Exp Med Biol 605:387–392. doi:10.1007/978-0-387-73693-8_68
56. Weese-Mayer DE, Lieske SP, Boothby CM, Kenny AS, Bennett HL, Silvestri JM, Ramirez JM (2006) Autonomic nervous system dysregulation: breathing and heart rate perturbation during wakefulness in young girls with Rett syndrome. Pediatr Res 60(4):443–449. doi:10.1203/01.pdr.0000238302.84552.d0
57. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K (2011) Optogenetics in neural systems. Neuron 71(1):9–34. doi:10.1016/j.neuron.2011.06.004
58. Yokota S, Tsumori T, Ono K, Yasui Y (2004) Glutamatergic pathways from the Kolliker-Fuse nucleus to the phrenic nucleus in the rat. Brain Res 995(1):118–130
59. Yokota S, Oka T, Tsumori T, Nakamura S, Yasui Y (2007) Glutamatergic neurons in the Kolliker-Fuse nucleus project to the rostral ventral respiratory group and phrenic nucleus: a combined retrograde tracing and in situ hybridization study in the rat. Neurosci Res 59(3):341–346. doi:10.1016/j.neures.2007.08.004
60. Yokota S, Niu JG, Tsumori T, Oka T, Yasui Y (2011) Glutamatergic Kolliker-Fuse nucleus neurons innervate hypoglossal motoneurons whose axons form the medial (protruder) branch of the hypoglossal nerve in the rat. Brain Res 1404:10–20. doi:10.1016/j.brainres.2011.06.025
61. Zhou Z, Champagnat J, Poon CS (1997) Phasic and long-term depression in brainstem nucleus tractus solitarius neurons: differing roles of AMPA receptor desensitization. J Neurosci 17(14):5349–5356