Permanent diaphragmatic deficits and spontaneous respiratory plasticity in a mouse model of incomplete cervical spinal cord injury

Alexandrov, 2007, Prefrontal control of respiration, J. Physiol. Pharmacol., 58, 17 Alilain, 2011, Functional regeneration of respiratory pathways after spinal cord injury, Nature, 475, 196, 10.1038/nature10199 Bennett, 1999, Spasticity in rats with sacral spinal cord injury, J. Neurotrauma, 16, 69, 10.1089/neu.1999.16.69 Bennett, 2004, Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury, J. Neurophysiol., 91, 2247, 10.1152/jn.00946.2003 Bezdudnaya, 2018, Spontaneous respiratory plasticity following unilateral high cervical spinal cord injury in behaving rats, Exp. Neurol., 305, 56, 10.1016/j.expneurol.2018.03.014 Boulenguez, 2010, Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury, Nat. Med., 16, 302, 10.1038/nm.2107 Burns, 2019, N-Acetylcysteine decreases fibrosis and increases force-generating capacity of mdx diaphragm, Antioxidants (Basel), 8, E581, 10.3390/antiox8120581 Cui, 2016, Defining preBötzinger complex rhythm- and pattern-generating neural microcircuits in vivo, Neuron, 91, 602, 10.1016/j.neuron.2016.07.003 Dougherty, 2018, Daily acute intermittent hypoxia improves breathing function with acute and chronic spinal injury via distinct mechanisms, Respir. Physiol. Neurobiol., 256, 50, 10.1016/j.resp.2017.05.004 ElMallah, 2015, Stimulation of respiratory motor output and ventilation in a murine model of pompe disease by ampakines, Am. J. Respir. Cell Mol. Biol., 53, 326, 10.1165/rcmb.2014-0374OC ElMallah, 2016, Power spectral analysis of hypoglossal nerve activity during intermittent hypoxia-induced long-term facilitation in mice, J. Neurophysiol., 115, 1372, 10.1152/jn.00479.2015 Feldman, 1985, Projections from the ventral respiratory group to phrenic and intercostal motoneurons in cat: an autoradiographic study, J. Neurosci., 5, 1993, 10.1523/JNEUROSCI.05-08-01993.1985 Feldman, 2013, Understanding the rhythm of breathing: so near, yet so far, Annu. Rev. Physiol., 75, 423, 10.1146/annurev-physiol-040510-130049 Freund, 1983, Motor unit and muscle activity in voluntary motor control, Physiol. Rev., 63, 387, 10.1152/physrev.1983.63.2.387 Fuller, 2003, Synaptic pathways to phrenic motoneurons are enhanced by chronic intermittent hypoxia after cervical spinal cord injury, J. Neurosci., 23, 2993, 10.1523/JNEUROSCI.23-07-02993.2003 Fuller, 2008, Modest spontaneous recovery of ventilation following chronic high cervical hemisection in rats, Exp. Neurol., 211, 97, 10.1016/j.expneurol.2008.01.013 Gandevia, 1987, Activation of the human diaphragm from the motor cortex, J. Physiol., 384, 109, 10.1113/jphysiol.1987.sp016445 Golder, 2005, Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury, J. Neurosci., 25, 2925, 10.1523/JNEUROSCI.0148-05.2005 Golder, 2001, Altered respiratory motor drive after spinal cord injury: supraspinal and bilateral effects of a unilateral lesion, J. Neurosci., 21, 8680, 10.1523/JNEUROSCI.21-21-08680.2001 Golder, 2003, Respiratory motor recovery after unilateral spinal cord injury: eliminating crossed phrenic activity decreases tidal volume and increases contralateral respiratory motor output, J. Neurosci., 23, 2494, 10.1523/JNEUROSCI.23-06-02494.2003 Goshgarian, 1981, The role of cervical afferent nerve fiber inhibition of the crossed phrenic phenomenon, Exp. Neurol., 72, 211, 10.1016/0014-4886(81)90139-4 Goshgarian, 2003, Invited review: the crossed phrenic phenomenon: a model for plasticity in the respiratory pathways following spinal cord injury, J. Appl. Physiol., 94, 795, 10.1152/japplphysiol.00847.2002 Gutierrez, 2013, Intermittent hypoxia training after C2 hemisection modifies the expression of PTEN and mTOR, Exp. Neurol., 248, 45, 10.1016/j.expneurol.2013.05.013 Hocker, 2019, Viral mimetic-induced inflammation abolishes Q-pathway, but not S-pathway, respiratory motor plasticity in adult rats, Front. Physiol., 10, 10.3389/fphys.2019.01039 Huang, 2009, Identification of the neural pathway underlying spontaneous crossed phrenic activity in neonatal rats, Neuroscience, 163, 1109, 10.1016/j.neuroscience.2009.07.011 Kastner, 2008, Are rodents an appropriate pre-clinical model for treating spinal cord injury? Examples from the respiratory system, Exp. Neurol., 213, 249, 10.1016/j.expneurol.2008.07.008 Kawamura, 1989, The clinical features of spasms in patients with a cervical cord injury, Paraplegia, 27, 222 Keomani, 2014, A murine model of cervical spinal cord injury to study post-lesional respiratory neuroplasticity, J. Vis. Exp., 10.3791/51235 Lane, 2011, Spinal respiratory motoneurons and interneurons, Respir. Physiol. Neurobiol., 179, 3, 10.1016/j.resp.2011.07.004 Lane, 2008, Cervical prephrenic interneurons in the normal and lesioned spinal cord of the adult rat, J. Comp. Neurol., 511, 692, 10.1002/cne.21864 Lane, 2009, Spinal circuitry and respiratory recovery following spinal cord injury, Respir. Physiol. Neurobiol., 169, 123, 10.1016/j.resp.2009.08.007 Lee, 2017, Compensatory function of the diaphragm after high cervical hemisection in the rat, J. Neurotrauma, 34, 2634, 10.1089/neu.2016.4943 Lee, 2013, Phrenic motoneuron discharge patterns following chronic cervical spinal cord injury, Exp. Neurol., 249, 20, 10.1016/j.expneurol.2013.08.003 Lee, 2014, Respiratory motor outputs following unilateral midcervical spinal cord injury in the adult rat, J. Appl. Physiol. (1985), 116, 395, 10.1152/japplphysiol.01001.2013 Li, 2004, Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats, J. Neurophysiol., 91, 767, 10.1152/jn.00788.2003 Lindstrom, 1977, Interpretation of myoelectric power spectra: a model and its applications, Proc. IEEE, 65, 653, 10.1109/PROC.1977.10544 Lipski, 1986, Short latency inputs to phrenic motoneurones from the sensorimotor cortex in the cat, Exp. Brain Res., 61, 280, 10.1007/BF00239518 Lovett-Barr, 2012, Repetitive intermittent hypoxia induces respiratory and somatic motor recovery after chronic cervical spinal injury, J. Neurosci., 32, 3591, 10.1523/JNEUROSCI.2908-11.2012 Mantilla, 2014, TrkB kinase activity is critical for recovery of respiratory function after cervical spinal cord hemisection, Exp. Neurol., 261, 190, 10.1016/j.expneurol.2014.05.027 Minor, 2006, Spinal cord injury-induced plasticity in the mouse—the crossed phrenic phenomenon, Exp. Neurol., 200, 486, 10.1016/j.expneurol.2006.02.125 Moreno, 1992, Identification of the axon pathways which mediate functional recovery of a paralyzed hemidiaphragm following spinal cord hemisection in the adult rat, Exp. Neurol., 116, 219, 10.1016/0014-4886(92)90001-7 Murray, 2011, Motoneuron excitability and muscle spasms are regulated by 5-HT2B and 5-HT2C receptor activity, J. Neurophysiol., 105, 731, 10.1152/jn.00774.2010 Nantwi, 1999, Spontaneous functional recovery in a paralyzed hemidiaphragm following upper cervical spinal cord injury in adult rats, Neurorehabil. Neural Rep., 13, 225, 10.1177/154596839901300404 Nicaise, 2012, Degeneration of phrenic motor neurons induces long-term diaphragm deficits following mid-cervical spinal contusion in mice, J. Neurotrauma, 29, 2748, 10.1089/neu.2012.2467 O’Halloran, 2002, Chronic intermittent asphyxia impairs rat upper airway muscle responses to acute hypoxia and asphyxia, Chest, 122, 269, 10.1378/chest.122.1.269 O’Hara, 1991, Quantitative assessment of phrenic nerve functional recovery mediated by the crossed phrenic reflex at various time intervals after spinal cord injury, Exp. Neurol., 111, 244, 10.1016/0014-4886(91)90012-2 Porter, 1895, The path of the respiratory impulse from the bulb to the phrenic nuclei, J. Physiol., 17, 455, 10.1113/jphysiol.1895.sp000553 Sandhu, 2009, Respiratory recovery following high cervical hemisection, Respir. Physiol. Neurobiol., 169, 94, 10.1016/j.resp.2009.06.014 Satkunendrarajah, 2018, Cervical excitatory neurons sustain breathing after spinal cord injury, Nature, 562, 419, 10.1038/s41586-018-0595-z Seven, 2013, Non-stationarity and power spectral shifts in EMG activity reflect motor unit recruitment in rat diaphragm muscle, Respir. Physiol. Neurobiol., 185, 400, 10.1016/j.resp.2012.08.020 Sköld, 1999, Spasticity after traumatic spinal cord injury: nature, severity, and location, Arch. Phys. Med. Rehabil., 80, 1548, 10.1016/S0003-9993(99)90329-5 Streeter, 2019, Molecular and histologic outcomes following spinal cord injury in spiny mice, Acomys cahirinus, J. Comp. Neurol., 528, 1535, 10.1002/cne.24836 Stuth, 2008, Anesthetic effects on synaptic transmission and gain control in respiratory control, Respir. Physiol. Neurobiol., 164, 151, 10.1016/j.resp.2008.05.007 Teppema, 2011, Anesthetics and control of breathing, Respir. Physiol. Neurobiol., 177, 80, 10.1016/j.resp.2011.04.006 Tian, 1998, Bötzinger-complex expiratory neurons monosynaptically inhibit phrenic motoneurons in the decerebrate rat, Exp. Brain Res., 122, 149, 10.1007/s002210050502 Vandeweerd, 2018, Retrograde neuroanatomical tracing of phrenic motor neurons in mice, J. Vis. Exp., 56758 Vinit, 2009, Descending bulbospinal pathways and recovery of respiratory motor function following spinal cord injury, Respir. Physiol. Neurobiol., 169, 115, 10.1016/j.resp.2009.08.004 Vinit, 2006, High cervical lateral spinal cord injury results in long-term ipsilateral hemidiaphragm paralysis, J. Neurotrauma, 23, 1137, 10.1089/neu.2006.23.1137 Wen, 2019, Modulation of serotonin and Adenosine 2A receptors on intermittent hypoxia-induced respiratory recovery following mid-cervical contusion in the rat, J. Neurotrauma, 36, 2991, 10.1089/neu.2018.6371 Windelborn, 2012, Glial activation in the spinal ventral horn caudal to cervical injury, Respir. Physiol. Neurobiol., 180, 61, 10.1016/j.resp.2011.10.011 Winslow, 2003, Effect of spinal cord injury on the respiratory system, Am. J. Phys. Med. Rehabil., 82, 803, 10.1097/01.PHM.0000078184.08835.01 Wu, 2017, A V0 core neuronal circuit for inspiration, Nat. Commun., 8, 10.1038/s41467-017-00589-2 Wu, 2020, 5-HT7 receptor inhibition enhances respiratory recovery following daily acute intermittent hypoxia in rats with chronic mid-cervical spinal cord contusion, Neurorehabil. Neural Repair, 34, 333, 10.1177/1545968320905806 Zanella, 2014, When norepinephrine becomes a driver of breathing irregularities: how intermittent hypoxia fundamentally alters the modulatory response of the respiratory network, J. Neurosci., 34, 36, 10.1523/JNEUROSCI.3644-12.2014 Zholudeva, 2017, Anatomical recruitment of spinal V2a interneurons into phrenic motor circuitry after high cervical spinal cord injury, J. Neurotrauma, 34, 3058, 10.1089/neu.2017.5045