Skip to main content

Neural Network Reconfigurations: Changes of the Respiratory Network by Hypoxia as an Example

  • Chapter
  • First Online:
The Plastic Brain

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1015))

Abstract

Neural networks, including the respiratory network, can undergo a reconfiguration process by just changing the number, the connectivity or the activity of their elements. Those elements can be either brain regions or neurons, which constitute the building blocks of macrocircuits and microcircuits, respectively. The reconfiguration processes can also involve changes in the number of connections and/or the strength between the elements of the network. These changes allow neural networks to acquire different topologies to perform a variety of functions or change their responses as a consequence of physiological or pathological conditions. Thus, neural networks are not hardwired entities, but they constitute flexible circuits that can be constantly reconfigured in response to a variety of stimuli. Here, we are going to review several examples of these processes with special emphasis on the reconfiguration of the respiratory rhythm generator in response to different patterns of hypoxia, which can lead to changes in respiratory patterns or lasting changes in frequency and/or amplitude.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

BDNF:

Brain-derived neurotrophic factor

CNS:

Central nervous system

D1/D2:

Dopamine receptors

EEG:

Electroencephalography

E:

Expiratory

FFA:

Flufenamic acid

fMRI:

Functional Magnetic resonance imaging

I:

Inspiratory

ICAN :

Ca2+-activated cationic current

INaP :

Persistent Na+ current

LTF:

Long-term facilitation

MEA:

Multielectrode array

NTS :

Nucleus tractus solitarius

PI:

Postinspiratory

preBötC:

Pre-Bötzinger complex

RVLM:

Rostral ventrolateral medulla

STP:

Short-term potentiation

References

  • Almado CE, Leão RM, Machado BH (2014) Intrinsic properties of rostral ventrolateral medulla presympathetic and bulbospinal respiratory neurons of juvenile rats are not affected by chronic intermittent hypoxia. Exp Physiol 99(7):937–950

    Article  PubMed  Google Scholar 

  • Armstrong GA, López-Guerrero JJ, Dawson-Scully K, Peña F, Robertson RM (2010) Inhibition of protein kinase G activity protects neonatal mouse respiratory network from hyperthermic and hypoxic stress. Brain Res 1311:64–72

    Article  CAS  PubMed  Google Scholar 

  • Bach KB, Mitchell GS (1996) Hypoxia-induced long-term facilitation of respiratory activity is serotonin dependent. Respir Physiol 104(2–3):251–260

    Article  CAS  PubMed  Google Scholar 

  • Ballanyi K, Völker A, Richter DW (1994) Anoxia induced functional inactivation of neonatal respiratory neurones in vitro. Neuroreport 6(1):165–168

    Article  CAS  PubMed  Google Scholar 

  • Ballanyi K, Onimaru H, Homma I (1999) Respiratory network function in the isolated brainstem-spinal cord of newborn rats. Prog Neurobiol 59(6):583–634

    Article  CAS  PubMed  Google Scholar 

  • Barnes BJ, Tuong CM, Mellen NM (2007) Functional imaging reveals respiratory network activity during hypoxic and opioid challenge in the neonate rat tilted sagittal slab preparation. J Neurophysiol 97(3):2283–2292

    Article  PubMed  Google Scholar 

  • Bassett DS, Meyer-Lindenberg A, Achard S, Duke T, Bullmore E (2006) Adaptive reconfiguration of fractal small-world human brain functional networks. Proc Natl Acad Sci U S A 103(51):19518–19523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker R, Braun U, Schwarz AJ, Gass N, Schweiger JI, Weber-Fahr W, Schenker E, Spedding M, Clemm von Hohenberg C, Risterucci C, Zang Z, Grimm O, Tost H, Sartorius A, Meyer-Lindenberg A (2016) Species-conserved reconfigurations of brain network topology induced by ketamine. Transl Psychiatry 6:e786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beggs JM, Plenz D (2004) Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J Neurosci 24(22):5216–5229

    Article  CAS  PubMed  Google Scholar 

  • Beidleman BA, Muza SR, Fulco CS, Cymerman A, Ditzler DT, Stulz D, Staab JE, Robinson SR, Skrinar GS, Lewis SF, Sawka MN (2003) Intermittent altitude exposures improve muscular performance at 4,300 m. J Appl Physiol (1985) 95(5):1824–1832

    Article  Google Scholar 

  • Belikova MV, Kolesnikova EE, Serebrovskaya TV (2012) Intermittent hypoxia and experimental Parkinson’s disease. In: Xi L, Serebrovskaya TV (eds) Intermittent hypoxia and human diseases. Springer, New York, pp 147–153

    Chapter  Google Scholar 

  • Blitz DM, Ramirez JM (2002) Long-term modulation of respiratory network activity following anoxia in vitro. J Neurophysiol 87(6):2964–2971

    PubMed  Google Scholar 

  • Brovelli A, Badier JM, Bonini F, Bartolomei F, Coulon O, Auzias G (2017) Dynamic reconfiguration of visuomotor-related functional connectivity networks. J Neurosci 37(4):839–853

    Article  CAS  PubMed  Google Scholar 

  • Cai XH, Zhou YH, Zhang CX, Hu LG, Fan XF, Li CC, Zheng GQ, Gong YS (2010) Chronic intermittent hypoxia exposure induces memory impairment in growing rats. Acta Neurobiol Exp (Wars) 70(3):279–287

    Google Scholar 

  • Cao C, Slobounov S (2010) Alteration of cortical functional connectivity as a result of traumatic brain injury revealed by graph theory, ICA, and sLORETA analyses of EEG signals. IEEE Trans Neural Syst Rehabil Eng 18(1):11–19

    Article  CAS  PubMed  Google Scholar 

  • Cao KY, Zwillich CW, Berthon-Jones M, Sullivan CE (1992) Increased normoxic ventilation induced by repetitive hypoxia in conscious dogs. J Appl Physiol (1985) 73(5):2083–2088

    CAS  Google Scholar 

  • Carrillo-Reid L, Tecuapetla F, Tapia D, Hernández-Cruz A, Galarraga E, Drucker-Colin R, Bargas J (2008) Encoding network states by striatal cell assemblies. J Neurophysiol 99(3):1435–1450

    Article  PubMed  Google Scholar 

  • Carrillo-Reid L, Hernández-López S, Tapia D, Galarraga E, Bargas J (2011) Dopaminergic modulation of the striatal microcircuit: receptor-specific configuration of cell assemblies. J Neurosci 31(42):14972–14983

    Article  CAS  PubMed  Google Scholar 

  • Carroll MS, Ramirez JM (2013) Cycle-by-cycle assembly of respiratory network activity is dynamic and stochastic. J Neurophysiol 109(2):296–305

    Article  PubMed  Google Scholar 

  • Carroll MS, Viemari JC, Ramirez JM (2013) Patterns of inspiratory phase-dependent activity in the in vitro respiratory network. J Neurophysiol 109(2):285–295

    Article  PubMed  Google Scholar 

  • Carter AR, Shulman GL, Corbetta M (2012) Why use a connectivity-based approach to study stroke and recovery of function? NeuroImage 62(4):2271–2280

    Article  PubMed  PubMed Central  Google Scholar 

  • Choi SH, Lee H, Chung TS, Park KM, Jung YC, Kim SI, Kim JJ (2012) Neural network functional connectivity during and after an episode of delirium. Am J Psychiatry 169(5):498–507

    Article  PubMed  Google Scholar 

  • Cohen JR, D’Esposito M (2016) The segregation and integration of distinct brain networks and their relationship to cognition. J Neurosci 36(48):12083–12094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen JR, Gallen CL, Jacobs EG, Lee TG, D’Esposito M (2014) Quantifying the reconfiguration of intrinsic networks during working memory. PLoS One 9(9):e106636

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Vico Fallani F, Richiardi J, Chavez M, Achard S (2014) Graph analysis of functional brain networks: practical issues in translational neuroscience. Philos Trans R Soc Lond B Biol Sci 369(1653):pii: 20130521

    Article  Google Scholar 

  • Del Negro CA, Morgado-Valle C, Feldman JL (2002) Respiratory rhythm: an emergent network property? Neuron 34(5):821–830

    Article  PubMed  Google Scholar 

  • Del Negro CA, Morgado-Valle C, Hayes JA, Mackay DD, Pace RW, Crowder EA, Feldman JL (2005) Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J Neurosci 25(2):446–453

    Article  PubMed  CAS  Google Scholar 

  • Dupret D, O’Neill J, Csicsvari J (2013) Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron 78(1):166–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • England SJ, Melton JE, Douse MA, Duffin J (1995) Activity of respiratory neurons during hypoxia in the chemodenervated cat. J Appl Physiol (1985) 78(3):856–861

    CAS  Google Scholar 

  • Flamm RE, Harris-Warrick RM (1986) Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit. J Neurophysiol 55(5):847–865

    CAS  PubMed  Google Scholar 

  • Flores-Martínez E, Peña-Ortega F (2017) Amyloid β peptide-induced changes in prefrontal cortex activity and its response to hippocampal input. Int J Pept 2017:7386809

    Article  PubMed  PubMed Central  Google Scholar 

  • Fregosi RF (1991) Short-term potentiation of breathing in humans. J Appl Physiol (1985) 71(3):892–899

    CAS  Google Scholar 

  • Fregosi RF, Mitchell GS (1994) Long-term facilitation of inspiratory intercostal nerve activity following carotid sinus nerve stimulation in cats. J Physiol 477(Pt 3):469–479

    Article  PubMed  PubMed Central  Google Scholar 

  • Gaiteri C, Rubin JE (2011) The interaction of intrinsic dynamics and network topology in determining network burst synchrony. Front Comput Neurosci 5:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Galán RF, Dick TE, Baekey DM (2010) Analysis and modeling of ensemble recordings from respiratory pre-motor neurons indicate changes in functional network architecture after acute hypoxia. Front Comput Neurosci 4:pii: 131

    Article  Google Scholar 

  • Gandolfi D, Mapelli J, D’Angelo E (2015) Long-term spatiotemporal reconfiguration of neuronal activity revealed by voltage-sensitive dye imaging in the cerebellar granular layer. Neural Plast 2015:284986

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Getting PA (1983) Neural control of swimming in Tritonia. Symp Soc Exp Biol 37:89–128

    CAS  PubMed  Google Scholar 

  • Gong XW, Li JB, Lu QC, Liang PJ, Zhang PM (2014) Effective connectivity of hippocampal neural network and its alteration in Mg2+-free epilepsy model. PLoS One 9(3):e92961

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gourévitch B, Mellen N (2014) The preBötzinger complex as a hub for network activity along the ventral respiratory column in the neonate rat. NeuroImage 98:460–474

    Article  PubMed  Google Scholar 

  • Gozal E, Row BW, Schurr A, Gozal D (2001) Developmental differences in cortical and hippocampal vulnerability to intermittent hypoxia in the rat. Neurosci Lett 305(3):197–201

    Article  CAS  PubMed  Google Scholar 

  • Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 100(1):253–258

    Article  CAS  PubMed  Google Scholar 

  • Griffin HS, Pugh K, Kumar P, Balanos GM (2012) Long-term facilitation of ventilation following acute continuous hypoxia in awake humans during sustained hypercapnia. J Physiol 590(Pt 20):5151–5165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffioen KJ, Kamendi HW, Gorini CJ, Bouairi E, Mendelowitz D (2007) Reactive oxygen species mediate central cardiorespiratory network responses to acute intermittent hypoxia. J Neurophysiol 97(3):2059–2066

    Article  PubMed  Google Scholar 

  • Guedj C, Monfardini E, Reynaud AJ, Farnè A, Meunier M, Hadj-Bouziane F (2016) Boosting norepinephrine transmission triggers flexible reconfiguration of brain networks at rest. Cereb Cortex (In press)

    Google Scholar 

  • Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Annu Rev Neurosci 14:39–57

    Article  CAS  PubMed  Google Scholar 

  • Hartelt N, Skorova E, Manzke T, Suhr M, Mironova L, Kügler S, Mironov SL (2008) Imaging of respiratory network topology in living brainstem slices. Mol Cell Neurosci 37(3):425–431

    Article  CAS  PubMed  Google Scholar 

  • Hayashi F, Coles SK, Bach KB, Mitchell GS, McCrimmon DR (1993) Time-dependent phrenic nerve responses to carotid afferent activation: intact vs. decerebellate rats. Am J Phys 265(4 Pt 2):R811–R819

    CAS  Google Scholar 

  • Hayashi F, Hinrichsen CF, McCrimmon DR (2003) Short-term plasticity of descending synaptic input to phrenic motoneurons in rats. J Appl Physiol (1985) 94(4):1421–1430

    Article  CAS  Google Scholar 

  • Hayes HB, Jayaraman A, Herrmann M, Mitchell GS, Rymer WZ, Trumbower RD (2014) Daily intermittent hypoxia enhances walking after chronic spinal cord injury: a randomized trial. Neurology 82(2):104–113

    Article  PubMed  PubMed Central  Google Scholar 

  • Hermans EJ, van Marle HJ, Ossewaarde L, Henckens MJ, Qin S, van Kesteren MT, Schoots VC, Cousijn H, Rijpkema M, Oostenveld R, Fernández G (2011) Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science 334(6059):1151–1153

    Article  CAS  PubMed  Google Scholar 

  • Hooper SL, Marder E (1987) Modulation of the lobster pyloric rhythm by the peptide proctolin. J Neurosci 7(7):2097–2112

    CAS  PubMed  Google Scholar 

  • Hooper SL, Moulins M (1990) Cellular and synaptic mechanisms responsible for a long-lasting restructuring of the lobster pyloric network. J Neurophysiol 64(5):1574–1589

    CAS  PubMed  Google Scholar 

  • Hunt CE (1992) The cardiorespiratory control hypothesis for sudden infant death syndrome. Clin Perinatol 19(4):757–771

    CAS  PubMed  Google Scholar 

  • Isla AG, Vázquez-Cuevas FG, Peña-Ortega F (2016) Exercise prevents amyloid-β-induced hippocampal network disruption by inhibiting GSK3β activation. J Alzheimers Dis 52(1):333–343

    Article  CAS  PubMed  Google Scholar 

  • Jáidar O, Carrillo-Reid L, Hernández A, Drucker-Colín R, Bargas J, Hernández-Cruz A (2010) Dynamics of the Parkinsonian striatal microcircuit: entrainment into a dominant network state. J Neurosci 30(34):11326–11336

    Article  PubMed  CAS  Google Scholar 

  • Klein JB, Gozal D, Pierce WM, Thongboonkerd V, Scherzer JA, Sachleben LR, Guo SZ, Cai J, Gozal E (2003) Proteomic identification of a novel protein regulated in CA1 and CA3 hippocampal regions during intermittent hypoxia. Respir Physiol Neurobiol 136(2–3):91–103

    Article  CAS  PubMed  Google Scholar 

  • Kline DD, Ramirez-Navarro A, Kunze DL (2007) Adaptive depression in synaptic transmission in the nucleus of the solitary tract after in vivo chronic intermittent hypoxia: evidence for homeostatic plasticity. J Neurosci 27(17):4663–4673

    Article  CAS  PubMed  Google Scholar 

  • Komiyama T, Sato TR, O’Connor DH, Zhang YX, Huber D, Hooks BM, Gabitto M, Svoboda K (2010) Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464(7292):1182–1186

    Article  CAS  PubMed  Google Scholar 

  • Koshiya N, Oku Y, Yokota S, Oyamada Y, Yasui Y, Okada Y (2014) Anatomical and functional pathways of rhythmogenic inspiratory premotor information flow originating in the pre-Bötzinger complex in the rat medulla. Neuroscience 268:194–211

    Article  CAS  PubMed  Google Scholar 

  • Lee DS, Badr MS, Mateika JH (2009a) Progressive augmentation and ventilator long-term facilitation are enhanced in sleep apnoea patients and are mitigated by antioxidant administration. J Physiol 587(Pt 22):5451–5467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KZ, Reier PJ, Fuller DD (2009b) Phrenic motoneuron discharge patterns during hypoxia-induced short-term potentiation in rats. J Neurophysiol 102(4):2184–2193

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee KZ, Sandhu MS, Dougherty BJ, Reier PJ, Fuller DD (2015) Hypoxia triggers short term potentiation of phrenic motoneuron discharge after chronic cervical spinal cord injury. Exp Neurol 263:314–324

    Article  CAS  PubMed  Google Scholar 

  • Lieske SP, Thoby-Brisson M, Telgkamp P, Ramirez JM (2000) Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps [see comment]. Nat Neurosci 3(6):600–607

    Article  CAS  PubMed  Google Scholar 

  • Lindsey BG, Morris KF, Segers LS, Shannon R (2000) Respiratory neuronal assemblies. Respir Physiol 122(2–3):183–196

    Article  CAS  PubMed  Google Scholar 

  • Liao W, Zhang Z, Mantini D, Xu Q, Ji GJ, Zhang H, Wang J, Wang Z, Chen G, Tian L, Jiao Q, Zang YF, Lu G (2014) Dynamical intrinsic functional architecture of the brain during absence seizures. Brain Struct Funct 219(6):2001–2015

    Article  PubMed  Google Scholar 

  • Lorea-Hernández JJ, Morales T, Rivera-Angulo AJ, Alcantara-Gonzalez D, Peña-Ortega F (2016) Microglia modulate respiratory rhythm generation and autoresuscitation. Glia 64(4):603–619

    Article  PubMed  Google Scholar 

  • Lovering AT, Fraigne JJ, Dunin-Barkowski WL, Vidruk EH, Orem JM (2006) Medullary respiratory neural activity during hypoxia in NREM and REM sleep in the cat. J Neurophysiol 95(2):803–810

    Article  PubMed  Google Scholar 

  • Lu XJ, Chen XQ, Weng J, Zhang HY, Pak DT, Luo JH, Du JZ (2009) Hippocampal spine-associated rap-specific GTPase-activating protein induces enhancement of learning and memory in postnatally hypoxia-exposed mice. Neuroscience 162(2):404–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lv Q, Yang L, Li G, Wang Z, Shen Z, Yu W, Jiang Q, Hou B, Pu J, Hu H, Wang Z (2016) Large-scale persistent network reconfiguration induced by ketamine in anesthetized monkeys: relevance to mood disorders. Biol Psychiatry 79(9):765–775

    Article  CAS  PubMed  Google Scholar 

  • Marder E (1994) Invertebrate neurobiology. Polymorphic neural networks. Curr Biol 4(8):752–754

    Article  CAS  PubMed  Google Scholar 

  • Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76(3):687–717

    CAS  PubMed  Google Scholar 

  • Marder E, Abbott LF, Turrigiano GG, Liu Z, Golowasch J (1996) Memory from the dynamics of intrinsic membrane currents. Proc Natl Acad Sci U S A 93(24):13481–13486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin RJ, Di Fiore JM, Macfarlane PM, Wilson CG (2012) Physiologic basis for intermittent hypoxic episodes in preterm infants. Adv Exp Med Biol 758:351–358

    Article  CAS  PubMed  Google Scholar 

  • Millet GP, Roels B, Schmitt L, Woorons X, Richalet JP (2010) Combining hypoxic methods for peak performance. Sports Med 40(1):1–25

    Article  PubMed  Google Scholar 

  • Mironov SL, Skorova E, Hartelt N, Mironova LA, Hasan MT, Kügler S (2009) Remodelling of the respiratory network in a mouse model of Rett syndrome depends on brain-derived neurotrophic factor regulated slow calcium buffering. J Physiol 587(Pt 11):2473–2485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell GS, Baker TL, Nanda SA, Fuller DD, Zabka AG, Hodgeman BA, Bavis RW, Mack KJ, Olson EB Jr (2001a) Invited review: intermittent hypoxia and respiratory plasticity. J Appl Physiol (1985) 90(6):2466–2475

    CAS  Google Scholar 

  • Mitchell GS, Powell FL, Hopkins SR, Milsom WK (2001b) Time domains of the hypoxic ventilatory response in awake ducks: episodic and continuous hypoxia. Respir Physiol 124(2):117–128

    Article  CAS  PubMed  Google Scholar 

  • Miyawaki T, Norimoto H, Ishikawa T, Watanabe Y, Matsuki N, Ikegaya Y (2014) Dopamine receptor activation reorganizes neuronal ensembles during hippocampal sharp waves in vitro. PLoS One 9(8):e104438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moraes DJ, da Silva MP, Bonagamba LG, Mecawi AS, Zoccal DB, Antunes-Rodrigues J, Varanda WA, Machado BH (2013) Electrophysiological properties of rostral ventrolateral medulla presympathetic neurons modulated by the respiratory network in rats. J Neurosci 33(49):19223–19237

    Article  CAS  PubMed  Google Scholar 

  • Morris KF, Gozal D (2004) Persistent respiratory changes following intermittent hypoxic stimulation in cats and human beings. Respir Physiol Neurobiol 140(1):1–8

    Article  PubMed  Google Scholar 

  • Morris KF, Baekey DM, Shannon R, Lindsey BG (2000) Respiratory neural activity during long-term facilitation. Respir Physiol 121(2–3):119–133

    Article  CAS  PubMed  Google Scholar 

  • Nagy F, Dickinson PS (1983) Control of a central pattern generator by an identified modulatory interneurone in crustacea. I. Modulation of the pyloric motor output. J Exp Biol 105:33–58

    CAS  PubMed  Google Scholar 

  • Nair D, Dayyat EA, Zhang SX, Wang Y, Gozal D (2011) Intermittent hypoxia-induced cognitive deficits are mediated by NADPH oxidase activity in a murine model of sleep apnea. PLoS One 6(5):e19847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nieto-Posadas A, Flores-Martínez E, Lorea-Hernández JJ, Rivera-Angulo AJ, Pérez-Ortega JE, Bargas J, Peña-Ortega F (2014) Change in network connectivity during fictive-gasping generation in hypoxia: prevention by a metabolic intermediate. Front Physiol 5:265

    Article  PubMed  PubMed Central  Google Scholar 

  • Nusbaum MP, Marder E (1989) A modulatory proctolin-containing neuron (MPN). II. State-dependent modulation of rhythmic motor activity. J Neurosci 9(5):1600–1607

    CAS  PubMed  Google Scholar 

  • Okada Y, Sasaki T, Oku Y, Takahashi N, Seki M, Ujita S, Tanaka KF, Matsuki N, Ikegaya Y (2012) Preinspiratory calcium rise in putative pre-Botzinger complex astrocytes. J Physiol 590(Pt 19):4933–4944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ott MM, Nuding SC, Segers LS, Lindsey BG, Morris KF (2011) Ventrolateral medullary functional connectivity and the respiratory and central chemoreceptor-evoked modulation of retrotrapezoid-parafacial neurons. J Neurophysiol 105(6):2960–2975

    Article  PubMed  PubMed Central  Google Scholar 

  • Parker D, Zhang W, Grillner S (1998) Substance P modulates NMDA responses and causes long-term protein synthesis-dependent modulation of the lamprey locomotor network. J Neurosci 18(12):4800–4813

    CAS  PubMed  Google Scholar 

  • Paton JF, Abdala AP, Koizumi H, Smith JC, St-John WM (2006) Respiratory rhythm generation during gasping depends on persistent sodium current. Nat Neurosci 9(3):311–313

    Article  CAS  PubMed  Google Scholar 

  • Payne RS, Goldbart A, Gozal D, Schurr A (2004) Effect of intermittent hypoxia on long-term potentiation in rat hippocampal slices. Brain Res 1029(2):195–199

    Article  CAS  PubMed  Google Scholar 

  • Peña F (2008) Contribution of pacemaker neurons to respiratory rhythms generation in vitro. Adv Exp Med Biol 605:114–118

    Article  PubMed  Google Scholar 

  • Peña F (2009) Neuronal network properties underlying the generation of gasping. Clin Exp Pharmacol Physiol 36(12):1218–1228

    Article  PubMed  CAS  Google Scholar 

  • Peña F, Aguileta MA (2007) Effects of riluzole and flufenamic acid on eupnea and gasping of neonatal mice in vivo. Neurosci Lett 415(3):288–293

    Article  PubMed  CAS  Google Scholar 

  • Peña F, García O (2006) Breathing generation and potential pharmacotherapeutic approaches to central respiratory disorders. Curr Med Chem 13(22):2681–2693

    Article  PubMed  Google Scholar 

  • Peña F, Parkis MA, Tryba AK, Ramirez JM (2004) Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43(1):105–117

    Article  PubMed  Google Scholar 

  • Peña F, Ramirez JM (2002) Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22(24):11055–11064

    PubMed  Google Scholar 

  • Peña F, Ramirez JM (2004) Substance P-mediated modulation of pacemaker properties in the mammalian respiratory network. J Neurosci 24(34):7549–7556

    Article  PubMed  CAS  Google Scholar 

  • Peña F, Ramirez JM (2005) Hypoxia-induced changes in neuronal network properties. Mol Neurobiol 32(3):251–283

    Article  PubMed  Google Scholar 

  • Peña F, Ordaz B (2008) Non-selective cation channel blockers: potential use in nervous system basic research and therapeutics. Mini Rev Med Chem 8(8):812–819

    Article  PubMed  Google Scholar 

  • Peña F, Meza-Andrade R, Páez-Zayas V, González-Marín MC (2008) Gasping generation in developing Swiss-Webster mice in vitro and in vivo. Neurochem Res 33(8):1492–1500

    Article  PubMed  CAS  Google Scholar 

  • Peña F, Ordaz B, Balleza-Tapia H, Bernal-Pedraza R, Márquez-Ramos A, Carmona-Aparicio L, Giordano M (2010) Beta-amyloid protein (25-35) disrupts hippocampal network activity: role of Fyn-kinase. Hippocampus 20(1):78–96

    PubMed  Google Scholar 

  • Peña-Ortega F (2012) Tonic neuromodulation of the inspiratory rhythm generator. Front Physiol 3:253

    Article  PubMed  PubMed Central  Google Scholar 

  • Peña-Ortega F (2013) Amyloid beta-protein and neural network dysfunction. J Neurodegener Dis 2013:657470

    PubMed  PubMed Central  Google Scholar 

  • Poets CF, Meny RG, Chobanian MR, Bonofiglo RE (1999) Gasping and other cardiorespiratory patterns during sudden infant deaths. Pediatr Res 45(3):350–354

    Article  CAS  PubMed  Google Scholar 

  • Ponten SC, Bartolomei F, Stam CJ (2007) Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol 118(4):918–927

    Article  CAS  PubMed  Google Scholar 

  • Powell FL, Milsom WK, Mitchell GS (1998) Time domains of the hypoxic ventilator response. Respir Physiol 112(2):123–134

    Article  CAS  PubMed  Google Scholar 

  • Qin J, Liu H, Wei M, Zhao K, Chen J, Zhu J, Shen X, Yan R, Yao Z, Lu Q (2017) Reconfiguration of hub-level community structure in depressions: a follow-up study via diffusion tensor imaging. J Affect Disord 207:305–312

    Article  PubMed  Google Scholar 

  • Ramirez JM (1998) Reconfiguration of the respiratory network at the onset of locust flight. J Neurophysiol 80(6):3137–3147

    CAS  PubMed  Google Scholar 

  • Ramirez JM, Quellmalz UJ, Wilken B, Richter DW (1998) The hypoxic response of neurones within the in vitro mammalian respiratory network. J Physiol 507(Pt 2):571–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramirez JM, Tryba AK, Peña F (2004) Pacemaker neurons and neuronal networks: an integrative view. Curr Opin Neurobiol 14(6):665–674

    Article  CAS  PubMed  Google Scholar 

  • Ramirez JM, Folkow LP, Blix AS (2007) Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu Rev Physiol 69:113–143

    Article  CAS  PubMed  Google Scholar 

  • Ramírez-Jarquín JO, Lara-Hernández S, López-Guerrero JJ, Aguileta MA, Rivera-Angulo AJ, Sampieri A, Vaca L, Ordaz B, Peña-Ortega F (2012) Somatostatin modulates generation of inspiratory rhythms and determines asphyxia survival. Peptides 34(2):360–372

    Article  PubMed  CAS  Google Scholar 

  • Richter DW, Bischoff A, Anders K, Bellingham M, Windhorst U (1991) Response of the medullary respiratory network of the cat to hypoxia. J Physiol 443:231–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivera-Angulo AJ, Peña-Ortega F (2014) Isocitrate supplementation promotes breathing generation, gasping, and autoresuscitation in neonatal mice. J Neurosci Res 92(3):375–388

    Article  CAS  PubMed  Google Scholar 

  • Roberts EL Jr, He J, Chih CP (1998) The influence of glucose on intracellular and extracellular pH in rat hippocampal slices during and after anoxia. Brain Res 783(1):44–50

    Article  CAS  PubMed  Google Scholar 

  • Rodman JR, Harris MB, Rudkin AH, St-John WM, Leiter JC (2006) Gap junction blockade does not alter eupnea or gasping in the juvenile rat. Respir Physiol Neurobiol 152(1):51–60

    Article  CAS  PubMed  Google Scholar 

  • Rothschild G, Cohen L, Mizrahi A, Nelken I (2013) Elevated correlations in neuronal ensembles of mouse auditory cortex following parturition. J Neurosci 33(31):12851–12861

    Article  CAS  PubMed  Google Scholar 

  • Row BW, Kheirandish L, Neville JJ, Gozal D (2002) Impaired spatial learning and hyperactivity in developing rats exposed to intermittent hypoxia. Pediatr Res 52(3):449–453

    Article  PubMed  Google Scholar 

  • Row BW, Liu R, Xu W, Kheirandish L, Gozal D (2003) Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am J Respir Crit Care Med 167(11):1548–1553

    Article  PubMed  Google Scholar 

  • Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52(3):1059–1069

    Article  PubMed  Google Scholar 

  • Runfeldt MJ, Sadovsky AJ, MacLean JN (2014) Acetylcholine functionally reorganizes neocortical microcircuits. J Neurophysiol 112(5):1205–1216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandhu MS, Baekey D, Mailing NG, Sanchez J, Reier PJ, Fuller DD (2015) Mid-cervical neuronal discharge patterns during and following hypoxia. J Neurophysiol 113(7):2091–2101

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Matsuki N, Ikegaya Y (2007) Metastability of active CA3 networks. J Neurosci 27(3):517–528

    Article  CAS  PubMed  Google Scholar 

  • Schmidt C, Bellingham MC, Richter DW (1995) Adenosinergic modulation of respiratory neurones and hypoxic responses in the anaesthetized cat. J Physiol 483(Pt 3):769–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schultz DH, Cole MW (2016) Higher intelligence is associated with less task-related brain network reconfiguration. J Neurosci 36(33):8551–8561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Serebrovskaya TV, Manukhina EB, Smith ML, Downey HF, Mallet RT (2008) Intermittent hypoxia: cause of or therapy for systemic hypertension? Exp Biol Med (Maywood) 233(6):627–650

    Article  CAS  Google Scholar 

  • 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(5032):726–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokołowska B, Pokorski M (2006) Ventilatory augmentation by acute intermittent hypoxia in the rabbit. J Physiol Pharmacol 57(Suppl 4):341–347

    PubMed  Google Scholar 

  • Srinivas KV, Jain R, Saurav S, Sikdar SK (2007) Small-world network topology of hippocampal neuronal network is lost, in an in vitro glutamate injury model of epilepsy. Eur J Neurosci 25(11):3276–3286

    Article  PubMed  Google Scholar 

  • St John WM (1999) Rostral medullary respiratory neuronal activities of decerebrate cats in eupnea, apneusis and gasping. Respir Physiol 116(1):47–65

    Article  CAS  PubMed  Google Scholar 

  • St John WM, Bianchi AL (1985) Responses of bulbospinal and laryngeal respiratory neurons to hypercapnia and hypoxia. J Appl Physiol (1985) 59(4):1201–1207

    CAS  Google Scholar 

  • Tadjalli A, Duffin J, Li YM, Hong H, Peever J (2007) Inspiratory activation is not required for episodic hypoxia-induced respiratory long-term facilitation in postnatal rats. J Physiol 585(Pt 2):593–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi N, Sasaki T, Matsumoto W, Matsuki N, Ikegaya Y (2010) Circuit topology for synchronizing neurons in spontaneously active networks. Proc Natl Acad Sci U S A 107(22):10244–10249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terada J, Nakamura A, Zhang W, Yanagisawa M, Kuriyama T, Fukuda Y, Kuwaki T (2008) Ventilatory long-term facilitation in mice can be observed during both sleep and wake periods and depends on orexin. J Appl Physiol (1985) 104(2):499–507

    Article  Google Scholar 

  • Tester NJ, Fuller DD, Fromm JS, Spiess MR, Behrman AL, Mateika JH (2014) Long-term facilitation of ventilation in humans with chronic spinal cord injury. Am J Respir Crit Care Med 189(1):57–65

    PubMed  PubMed Central  Google Scholar 

  • Thoby-Brisson M, Simmers J (1998) Neuromodulatory inputs maintain expression of a lobster motor pattern-generating network in a modulation-dependent state: evidence from long-term decentralization in vitro. J Neurosci 18(6):2212–2225

    CAS  PubMed  Google Scholar 

  • Thoby-Brisson M, Ramirez JM (2000) Role of inspiratory pacemaker neurons in mediating the hypoxic response of the respiratory network in vitro. J Neurosci 20(15):5858–5866

    CAS  PubMed  Google Scholar 

  • Trumbower RD, Jayaraman A, Mitchell GS, Rymer WZ (2012) Exposure to acute intermittent hypoxia augments somatic motor function in humans with incomplete spinal cord injury. Neurorehabil Neural Repair 26(2):163–172

    Article  PubMed  Google Scholar 

  • Tsai YW, Yang YR, Wang PS, Wang RY (2011) Intermittent hypoxia after transient focal ischemia induces hippocampal neurogenesis and c-Fos expression and reverses spatial memory deficits in rats. PLoS One 6(8):e24001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai YW, Yang YR, Sun SH, Liang KC, Wang RY (2013) Post ischemia intermittent hypoxia induces hippocampal neurogenesis and synaptic alterations and alleviates long-term memory impairment. J Cereb Blood Flow Metab 33(5):764–773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner DL, Mitchell GS (1997) Long-term facilitation of ventilation following repeated hypoxic episodes in awake goats. J Physiol 499(Pt 2):543–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vargas-Barroso V, Ordaz-Sánchez B, Peña-Ortega F, Larriva-Sahd JA (2016) Electrophysiological Evidence for a Direct Link between the Main and Accessory Olfactory Bulbs in the Adult Rat. Front Neurosci 9:518

    Article  PubMed  PubMed Central  Google Scholar 

  • Wall AM, Corcoran AE, O’Halloran KD, O’Connor JJ (2014) Effects of prolyl-hydroxylase inhibition and chronic intermittent hypoxia on synaptic transmission and plasticity in the rat CA1 and dentate gyrus. Neurobiol Dis 62:8–17

    Article  CAS  PubMed  Google Scholar 

  • Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393(6684):440–442

    Article  CAS  PubMed  Google Scholar 

  • Xie H, Yung WH (2012) Chronic intermittent hypoxia-induced deficits in synaptic plasticity and neurocognitive functions: a role for brain-derived neurotrophic factor. Acta Pharmacol Sin 33(1):5–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie H, Leung KL, Chen L, Chan YS, Ng PC, Fok TF, Wing YK, Ke Y, Li AM, Yung WH (2010) Brain-derived neurotrophic factor rescues and prevents chronic intermittent hypoxia-induced impairment of hippocampal long-term synaptic plasticity. Neurobiol Dis 40(1):155–162

    Article  CAS  PubMed  Google Scholar 

  • Yuan Q, Isaacson JS, Scanziani M (2011) Linking neuronal ensembles by associative synaptic plasticity. PLoS One 6(6):e20486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zanella S, Doi A, Garcia AJ 3rd, Elsen F, Kirsch S, Wei AD, Ramirez JM (2014) When norepinephrine becomes a driver of breathing irregularities: how intermittent hypoxia fundamentally alters the modulatory response of the respiratory network. J Neurosci 34(1):36–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zavala-Tecuapetla C, Aguileta MA, Lopez-Guerrero JJ, González-Marín MC, Peña F (2008) Calcium-activated potassium currents differentially modulate respiratory rhythm generation. Eur J Neurosci 27(11):2871–2884

    Article  CAS  PubMed  Google Scholar 

  • Zavala-Tecuapetla C, Tapia D, Rivera-Angulo AJ, Galarraga E, Peña-Ortega F (2014) Morphological characterization of respiratory neurons in the pre-Bötzinger complex. Prog Brain Res 209:39–56

    Article  PubMed  Google Scholar 

  • Zhang JX, Chen XQ, Du JZ, Chen QM, Zhu CY (2005) Neonatal exposure to intermittent hypoxia enhances mice performance in water maze and 8-arm radial maze tasks. J Neurobiol 65(1):72–84

    Article  PubMed  Google Scholar 

  • Zhang J, Cheng W, Liu Z, Zhang K, Lei X, Yao Y, Becker B, Liu Y, Kendrick KM, Lu G, Feng J (2016) Neural, electrophysiological and anatomical basis of brain-network variability and its characteristic changes in mental disorders. Brain 139(Pt 8):2307–2321

    Article  PubMed  Google Scholar 

  • Zhu WZ, Xie Y, Chen L, Yang HT, Zhou ZN (2006) Intermittent high altitude hypoxia inhibits opening of mitochondrial permeability transition pores against reperfusion injury. J Mol Cell Cardiol 40(1):96–106

    Article  CAS  PubMed  Google Scholar 

  • Zhu XH, Yan HC, Zhang J, Qu HD, Qiu XS, Chen L, Li SJ, Cao X, Bean JC, Chen LH, Qin XH, Liu JH, Bai XC, Mei L, Gao TM (2010) Intermittent hypoxia promotes hippocampal neurogenesis and produces antidepressant-like effects in adult rats. J Neurosci 30(38):12653–12663

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Dorothy Pless and Jessica González for editorial comments. This study was supported by Fundación Marcos Moshinsky, CONACyT Grants 117, 151261, 235789, 24688 and 181323; and by DGAPA-UNAM Grants IN200715.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fernando Peña-Ortega .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Peña-Ortega, F. (2017). Neural Network Reconfigurations: Changes of the Respiratory Network by Hypoxia as an Example. In: von Bernhardi, R., Eugenín, J., Muller, K. (eds) The Plastic Brain. Advances in Experimental Medicine and Biology, vol 1015. Springer, Cham. https://doi.org/10.1007/978-3-319-62817-2_12

Download citation

Publish with us

Policies and ethics