SpringerLink
Log in

Glutamate, Glutamine, GABA and Oxidative Products in the Pons Following Cortical Injury and Their Role in Motor Functional Recovery

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Brain injury leads to an excitatory phase followed by an inhibitory phase in the brain. The clinical sequelae caused by cerebral injury seem to be a response to remote functional inhibition of cerebral nuclei located far from the motor cortex but anatomically related to the injury site. It appears that such functional inhibition is mediated by an increase in lipid peroxidation (LP). To test this hypothesis, we report data from 80 rats that were allocated to the following groups: the sham group (n = 40), in which rats received an intracortical infusion of artificial cerebrospinal fluid (CSF); the injury group (n = 20), in which rats received CSF containing ferrous chloride (FeCl2, 50 mM); and the recovery group (n = 20), in which rats were injured and allowed to recover. Beam-walking, sensorimotor and spontaneous motor activity tests were performed to evaluate motor performance after injury. Lipid fluorescent products (LFPs) were measured in the pons. The total pontine contents of glutamate (GLU), glutamine (GLN) and gamma-aminobutyric acid (GABA) were also measured. In injured rats, the motor deficits, LFPs and total GABA and GLN contents in the pons were increased, while the GLU level was decreased. In contrast, in recovering rats, none of the studied variables were significantly different from those in sham rats. Thus, motor impairment after cortical injury seems to be mediated by an inhibitory pontine response, and functional recovery may result from a pontine restoration of the GLN–GLU–GABA cycle, while LP may be a primary mechanism leading to remote pontine inhibition after cortical injury.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The data set analyzed during the current study is available from the corresponding author on reasonable request.

Code Availability

Not applicable.

References

  1. Bueno-Nava A, Montes S, DelaGarza-Montano P, Alfaro-Rodriguez A, Ortiz A, Gonzalez-Pina R (2008) Reversal of noradrenergic depletion and lipid peroxidation in the pons after brain injury correlates with motor function recovery in rats. Neurosci Lett 443:32–36

    Article  CAS  PubMed  Google Scholar 

  2. Kim Y, Kim S-H, Kim J-S, Hong BY (2018) Modification of Cerebellar Afferent Pathway in the Subacute Phase of Stroke. J Stroke Cerebrovasc Dis 27:2445–2452

    Article  PubMed  Google Scholar 

  3. Hayes JP, Bigler ED, Verfaellie M (2016) Traumatic brain injury as a disorder of brain connectivity. J Int Neuropsychol Soc 22:120–137

    Article  PubMed  PubMed Central  Google Scholar 

  4. Kim Y, Lim SH, Park GY (2019) Crossed cerebellar diaschisis has an adverse effect on functional outcome in the subacute rehabilitation phase of stroke: a case-control study. Arch Phys Med Rehabil 100:1308–1316

    Article  PubMed  Google Scholar 

  5. Kim JS, Kim S-H, Lim SH, Im S, Hong BY, Oh J, Kim Y (2019) Degeneration of the inferior cerebellar peduncle after middle cerebral artery stroke. Stroke 50:2700–2707

    Article  CAS  PubMed  Google Scholar 

  6. Gonzalez-Pina R, Bueno-Nava A, Montes S, Alfaro-Rodriguez A, Gonzalez-Maciel A, Reynoso-Robles R, Ayala-Guerrero F (2006) Pontine and cerebellar norepinephrine content in adult rats recovering from focal cortical injury. Neurochem Res 31:1443–1449

    Article  CAS  PubMed  Google Scholar 

  7. Ramos-Languren LE, González-Piña R, Montes S, Chávez-García N, Ávila-Luna A, Barón-Flores V, Ríos C (2016) Sensorimotor recovery from cortical injury is accompanied by changes on norepinephrine and serotonin levels in the dentate gyrus and pons. Behav Brain Res 1(297):297–306

    Article  CAS  Google Scholar 

  8. Zhang D, **ao M, Wang L, Jia W (2019) Blood-based glutamate scavengers reverse traumatic brain injury-induced synaptic plasticity disruption by decreasing glutamate level in hippocampus interstitial fluid, but not cerebral spinal fluid, in vivo. Neurotox Res 35:360–372

    Article  CAS  PubMed  Google Scholar 

  9. Hovda DA, Fenney DM (1984) Amphetamine with experience promotes recovery of locomotor function after unilateral frontal cortex injury in the cat. Brain Res 298:358–361

    Article  CAS  PubMed  Google Scholar 

  10. Liu W, Li R, Yin J, Guo S, Chen Y, Fan H, Li G, Li Z, Li X, Zhang X, He X, Duan C (2019) Mesenchymal stem cells alleviate the early brain injury of subarachnoid hemorrhage partly by suppression of Notch1-dependent neuroinflammation: involvement of Botch. J Neuroinflammation 16:8

    Article  PubMed  PubMed Central  Google Scholar 

  11. Suzuki H (2015) What is early brain injury? Transl Stroke Res 6:1–3

    Article  PubMed  Google Scholar 

  12. Yang S, Chen X, Li S, Sun B, Hang C (2018) Melatonin treatment regulates SIRT3 Expression in early brain injury (EBI) due to Reactive oxygen species (ROS) in a mouse model of Subarachnoid hemorrhage (SAH). Med Sci Monit 24:3804–3814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Goldstein LB (2000) Effects of amphetamines and small related molecules on recovery after stroke in animals and man. Neuropharmacology 39:852–859

    Article  CAS  PubMed  Google Scholar 

  14. Boyeson MG, Feeney DM (1990) Intraventricular norepinephrine facilitates motor recovery following sensorimotor cortex injury. Pharmacol Biochem Behav 35:497–501

    Article  CAS  PubMed  Google Scholar 

  15. Boyeson MG, Krobert KA (1992) Cerebellar norepinephrine infusions facilitate recovery after sensorimotor cortex injury. Brain Res Bull 29:435–439

    Article  CAS  PubMed  Google Scholar 

  16. Mattson MP (2008) Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann N Y Acad Sci 1144:97–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Guerriero RM, Giza CC, Rotenberg A (2015) Glutamate and GABA imbalance following traumatic brain injury. Curr Neurol Neurosci Rep. https://doi.org/10.1007/s11910-015-0545-1

    Article  PubMed  PubMed Central  Google Scholar 

  18. Brailowsky S, Knight RT, Blood K, Scabini D (1986) gamma-Aminobutyric acid-induced potentiation of cortical hemiplegia. Brain Res 362:322–330

    Article  CAS  PubMed  Google Scholar 

  19. Katz DI, Alexander MP, Klein RB (1998) Recovery of arm function in patients with paresis after traumatic brain injury. Arch Phys Med Rehabil 79:488–493

    Article  CAS  PubMed  Google Scholar 

  20. Niimura K, Chugani DC, Muzik O, Chugani HT (1999) Cerebellar reorganization following cortical injury in humans: effects of lesion size and age. Neurology 52:792–797

    Article  CAS  PubMed  Google Scholar 

  21. Yasen AL, Smith J, Christie AD (2018) Glutamate and GABA concentrations following mild traumatic brain injury: a pilot study. J Neurophysiol 120:1318–1322

    Article  PubMed  Google Scholar 

  22. O’Dell DM, Gibson CJ, Wilson MS, DeFord SM, Hamm RJ (2000) Positive and negative modulation of the GABA(A) receptor and outcome after traumatic brain injury in rats. Brain Res 861:325–332

    Article  CAS  PubMed  Google Scholar 

  23. Cenni G, Blandina P, Mackie K, Nosi D, Formigli L, Giannoni P, Ballini C, Della Corte L, Mannaioni PF, Passani MB (2006) Differential effect of cannabinoid agonists and endocannabinoids on histamine release from distinct regions of the rat brain. Eur J Neurosci 24:1633–1644

    Article  PubMed  PubMed Central  Google Scholar 

  24. Anthonymuthu TS, Kenny EM, Bayır H (2016) Therapies targeting lipid peroxidation in traumatic brain injury. Brain Res 1640:57–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Krobert KA, Sutton RL, Feeney DM (1994) Spontaneous and amphetamine-evoked release of cerebellar noradrenaline after sensorimotor cortex contusion: an in vivo microdialysis study in the awake rat. J Neurochem 62:2233–2240

    Article  CAS  PubMed  Google Scholar 

  26. Serteser M, Úzben T, Gümüslü S, Balkan S, Balkan E (2001) Biochemical evidence of crossed cerebellar diaschisis in terms of nitric oxide indicators and lipid peroxidation products in rats during focal cerebral ischemia. Acta Neurol Scand 103:43–48

    Article  CAS  PubMed  Google Scholar 

  27. Daskalakis ZJ, Paradiso GO, Christensen BK, Fitzgerald PB, Gunraj C, Chen R (2004) Exploring the connectivity between the cerebellum and motor cortex in humans. J Physiol 557:689–700

    Article  CAS  PubMed  Google Scholar 

  28. Thompson KJ, Shoham S, Connor JR (2001) Iron and neurodegenerative disorders. Brain Res Bull 55:155–164

    Article  CAS  PubMed  Google Scholar 

  29. D’Ambrosio R, Perucca E (2004) Epilepsy after head injury. Curr Opin Neurol 17:731–735

    Article  PubMed  PubMed Central  Google Scholar 

  30. Davies KJA (1995) Oxidative stress: the paradox of aerobic life. Biochem Soc Symp 61:1–31

    Article  CAS  PubMed  Google Scholar 

  31. Halliwell B (1987) Oxidants and human disease: some new concepts. FASEB J 1:358–364

    Article  CAS  PubMed  Google Scholar 

  32. Murakami T, Takemori K, Yoshizumi H (1995) Prediction of stroke lesions in stroke-prone spontaneously hypertensive rats by glutathione peroxidase in erythrocytes. Biosci Biotechnol Biochem 59:1459–1463

    Article  CAS  PubMed  Google Scholar 

  33. Biagini G, Zoli M, Torri C, Boschi S, Vantaggiato G, Ballestri M, Baraldi A, Agnati LF (1997) Protective effects of delapril, indapamide and their combination chronically administered to stroke-prone spontaneously hypertensive rats fed a high-sodium diet. Clin Sci (Lond) 93:401–411

    Article  CAS  Google Scholar 

  34. Tejada S, Sureda A, Roca C, Gamundí A, Esteban S (2007) Antioxidant response and oxidative damage in brain cortex after high dose of pilocarpine. Brain Res Bullet 71:372–375

    Article  CAS  Google Scholar 

  35. Santos PSd, Costa JP, Tomé AdR, Saldanha GB, de Souza GF, Feng D, de Freitas RM (2011) Oxidative stress in rat striatum after pilocarpine-induced seizures is diminished by alpha-tocopherol. Eur J Pharmacol 668:65–71

    Article  PubMed  CAS  Google Scholar 

  36. Fabene PF, Merigo F, Benati D, Farace P, Nicolato E, Marzola P, Sbarbati A (2007) Pilocarpine-induced status epilepticus in rats involves ischemic and excitotoxic mechanisms. PloS One 2:e1105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Biagini G, Baldelli E, Longo D, Contri MB, Guerrini U, Sironi L, Gelosa P, Zini I, Ragsdale DS, Avoli M (2008) Proepileptic influence of a focal vascular lesion affecting entorhinal cortex-CA3 connections after status epilepticus. J Neuropathol Exp Neurol 67:687–701

    Article  PubMed  Google Scholar 

  38. Feeney DM, Baron JC (1986) Diaschisis. Stroke 17:817–830

    Article  CAS  PubMed  Google Scholar 

  39. Goldstein LB (2006) Neurotransmitters and motor activity: effects on functional recovery after brain injury. NeuroRx 3:451–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Maharaj DS, Limson JL, Daya S (2003) 6-Hydroxymelatonin converts Fe (III) to Fe (II) and reduces iron-induced lipid peroxidation. Life Sci 72:1367–1375

    Article  CAS  PubMed  Google Scholar 

  41. Halliwell B, Gutteridge JMC (1997) Lipid peroxidation in brain homogenates: the role of iron and hydroxyl radicals. J Neurochem 69:1330–1330

    Article  CAS  PubMed  Google Scholar 

  42. Zhang Y, Lu X, Tai B, Li W, Li T (2021) Ferroptosis and its multifaceted roles in cerebral stroke. Front Cell Neurosci 15:1–10

    Article  Google Scholar 

  43. She X, Lan B, Tian H, Tang B (2020) Cross talk between ferroptosis and cerebral ischemia. Front Neurosci 14:1–9

    Article  Google Scholar 

  44. Festing MF (2018) On determining sample size in experiments involving laboratory animals. Lab Anim 52:341–350

    Article  CAS  PubMed  Google Scholar 

  45. Harris JL, Yeh HW, Choi IY, Lee P, Berman NE, Swerdlow RH, Craciunas SC, Brooks WM (2012) Altered neurochemical profile after traumatic brain injury: H-1-MRS biomarkers of pathological mechanisms. J Cereb Blood Flow Metab 32:2122–2134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Olfert E, Cross B, Mc William A (1993) Guide for the care and use of experimental animals. Can Council Animal Care 1:211

    Google Scholar 

  47. NOM-062-ZOO-1999 (2001) Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio. In. Diario Oficial de la Federación.

  48. Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66:23–38

    Article  Google Scholar 

  49. Paxinos G, Watson C (1982) WITHDRAWN: Plates and Figures. In: Paxinos G, Watson C (eds) The Rat Brain in Stereotaxic Coordinates. Academic Press, USA, pp 13–153

    Chapter  Google Scholar 

  50. Bueno-Nava A, Gonzalez-Pina R, Alfaro-Rodriguez A, Nekrassov-Protasova V, Durand-Rivera A, Montes S, Ayala-Guerrero F (2010) Recovery of motor deficit, cerebellar serotonin and lipid peroxidation levels in the cortex of injured rats. Neurochem Res 35:1538–1545

    Article  CAS  PubMed  Google Scholar 

  51. Garcia JH, Wagner S, Liu K-F, Hu X-j (1995) Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Stroke 26:627–635

    Article  CAS  PubMed  Google Scholar 

  52. Triggs WJ, Willmore LJ (1984) In vivo lipid-peroxidation in rat-brain following intracortical Fe-2+ injection. J Neurochem 42:976–980

    Article  CAS  PubMed  Google Scholar 

  53. Santamaría A, Ríos C (1993) MK-801, an N-methyl-d-aspartate receptor antagonist, blocks quinolinic acid-induced lipid-peroxidation in rat corpus striatum. Neurosci Lett 159:51–54

    Article  PubMed  Google Scholar 

  54. Montes S, Alcaraz-Zubeldia M, Muriel P, Rios C (2003) Role of manganese accumulation in increased brain glutamine of the cirrhotic rat. Neurochem Res 28:911–917

    Article  CAS  PubMed  Google Scholar 

  55. González-Piña R, Paz C (1997) Brain monoamine changes in rats after short periods of ozone exposure. Neurochem Res. https://doi.org/10.1023/A:1027329405112

    Article  PubMed  Google Scholar 

  56. Ahmad SO, Baun J, Tipton B, Tate Y, Switzer RC (2019) Modification of AgNOR staining to reveal the nucleolus in thick sections specified for stereological and pathological assessments of brain tissue. Heliyon. https://doi.org/10.1016/j.heliyon.2019.e03047

    Article  PubMed  PubMed Central  Google Scholar 

  57. Gaschler MM, Stockwell BR (2017) Lipid peroxidation in cell death. Biochem Biophys Res Commun 482:419–425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Hall ED, Wang JA, Miller DM, Cebak JE, Hill RL (2019) Newer pharmacological approaches for antioxidant neuroprotection in traumatic brain injury. Neuropharmacology 145:247–258

    Article  CAS  PubMed  Google Scholar 

  59. Walls AB, Waagepetersen HS, Bak LK, Schousboe A, Sonnewald U (2015) The glutamine–glutamate/GABA cycle: function, regional differences in glutamate and GABA production and effects of interference with GABA metabolism. Neurochem Res 40:402–409

    Article  CAS  PubMed  Google Scholar 

  60. Gu F, Chauhan V, Chauhan A (2015) Glutathione redox imbalance in brain disorders. Curr Opin Clin Nutr Metab Care 18:89–95

    Article  CAS  PubMed  Google Scholar 

  61. Rafalowska U, Liu G-J, Floyd RA (1989) Peroxidation induced changes in synaptosomal transport of dopamine and γ-aminobutyric acid. Free Radical Biol Med 6:485–492

    Article  CAS  Google Scholar 

  62. Folkersma H, Foster Dingley JC, van Berckel BN, Rozemuller A, Boellaard R, Huisman MC, Lammertsma AA, Vandertop WP, Molthoff CF (2011) Increased cerebral (R)-[11C]PK11195 uptake and glutamate release in a rat model of traumatic brain injury: a longitudinal pilot study. J Neuroinflammation 8:67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Amorini AM, Lazzarino G, Di Pietro V, Signoretti S, Belli A, Tavazzi B (2017) Severity of experimental traumatic brain injury modulates changes in concentrations of cerebral free amino acids. J Cell Mol Med 21:530–542

    Article  CAS  PubMed  Google Scholar 

  64. Vespa P, Prins M, Ronne-Engstrom E, Caron M, Shalmon E, Hovda DA, Martin NA, Becker DP (1998) Increase in extracellular glutamate caused by reduced cerebral perfusion pressure and seizures after human traumatic brain injury: a microdialysis study. J Neurosurg 89:971–982

    Article  CAS  PubMed  Google Scholar 

  65. Chamoun R, Suki D, Gopinath SP, Goodman JC, Robertson C (2010) Role of extracellular glutamate measured by cerebral microdialysis in severe traumatic brain injury. J Neurosurg 113:564–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Henry LC, Tremblay S, Boulanger Y, Ellemberg D, Lassonde M (2010) Neurometabolic changes in the acute phase after sports concussions correlate with symptom severity. J Neurotrauma 27:65–76

    Article  PubMed  Google Scholar 

  67. Xu S, Zhuo JC, Racz J, Shi D, Roys S, Fiskum G, Gullapalli R (2011) Early microstructural and metabolic changes following controlled cortical impact injury in rat: a magnetic resonance imaging and spectroscopy study. J Neurotrauma 28:2091–2102

    Article  PubMed  PubMed Central  Google Scholar 

  68. Diaz-Ruiz A, Salgado-Ceballos H, Montes S, Maldonado V, Tristan L, Alcaraz-Zubeldia M, Ríos C (2007) Acute alterations of glutamate, glutamine, GABA, and other amino acids after spinal cord contusion in rats. Neurochem Res 32:57–63

    Article  CAS  PubMed  Google Scholar 

  69. MaI A-S, Medina MÁ (1999) Glutamine, as a precursor of glutathione, and oxidative stress. Mol Genet Metab 67:100–105

    Article  Google Scholar 

  70. Petito CK, Chung MC, Verkhovsky LM, Cooper AJL (1992) Brain glutamine synthetase increases following cerebral ischemia in the rat. Brain Res 569:275–280

    Article  CAS  PubMed  Google Scholar 

  71. Kim YK, Yang EJ, Cho K, Lim JY, Paik N-J (2014) Functional recovery after ischemic stroke is associated with reduced GABAergic inhibition in the cerebral cortex: a GABA PET study. Neurorehabil Neural Repair 28:576–583

    Article  PubMed  Google Scholar 

  72. Aston-Jones G, Rajkowski J, Cohen J (2000) Locus coeruleus and regulation of behavioral flexibility and attention. In: Aston-Jones G, Rajkowski J, Cohen J (eds) Progress in Brain Research. Elsevier, Amsterdam, pp 165–182

    Google Scholar 

  73. Lai YY, Clements JR, Siegel JM (1993) Glutamatergic and cholinergic projections to the pontine inhibitory area identified with horseradish peroxidase retrograde transport and immunohistochemistry. Journal of Comparative Neurology 336:321–330

    Article  CAS  PubMed  Google Scholar 

  74. Urrutia PJ, Bórquez DA, Núñez MT (2021) Inflaming the brain with iron. Antioxidants 10:1–27

    Article  CAS  Google Scholar 

  75. Petrova J, Manolov V, Vasilev V, Tzatchev K, Marinov B (2016) Ischemic stroke, inflammation, iron overload—Connection to a hepcidin. Int J Stroke. https://doi.org/10.1177/1747493015607509

    Article  PubMed  Google Scholar 

  76. Daglas M, Adlard PA (2018) The involvement of iron in traumatic brain injury and neurodegenerative disease. Front Neurosci. https://doi.org/10.3389/fnins.2018.00981

    Article  PubMed  PubMed Central  Google Scholar 

  77. Rahman AA, Amruta N, Pinteaux E, Bix GJ (2021) Neurogenesis after stroke: a therapeutic perspective. Transl Stroke Res 12:1–14

    Article  CAS  PubMed  Google Scholar 

  78. Zhang ZG, Chopp M (2009) Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol 8:491–500

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We wish to thank Tania Galván-Arrieta for her collaboration in the preparation of tables and figures.

Funding

This work was supported by  PAPIIT-UNAM (Grant: IA203319 to L.E.R.-L.) and the National Council of Science and Technology CONACYT (Grant: CB 2016-287614-M to R.G.-P. and A.B.-N.).

Author information

Authors and Affiliations

  1. Laboratory of Aging Biology, National Geriatric Institute, Av. Contreras 428 Col. San Jerónimo Lídice Alcaldía Magdalena Contreras, 10200, Mexico City, Mexico

    Rigoberto González-Piña

  2. Faculty of Psychology, Coordination of Psychobiology and Neurosciences, National Autonomous University of Mexico, Av. Universidad 3040 Col, Copilco Universidad Alcaldía Coyoacán, 04510, Mexico City, Mexico

    Laura E. Ramos-Languren

  3. National Institute of Rehabilitation LGII, Calz. Mexico-Xochimilco #289 Col. Arenal de Guadalupe Alcaldía Tlalpan, 14389, Mexico City, Mexico

    Alberto Avila-Luna, Carmen Parra-Cid & Antonio Bueno-Nava

  4. Section of Postgraduate Studies and Research, High Medical School, IPN. Salvador Diaz Miron Alcaldia Miguel Hidalgo, 11340, Mexico City, Mexico

    Gabriela García-Díaz & Rigoberto González-Piña

  5. School of Physical Culture, University of Holguín, Avenida XX Aniversario, 80100, Holguín, Cuba

    Roberto Rodríguez-Labrada

  6. Cuban Centre for Neurosciences, Calle 190 entre 25 y 27, Playa, 11300, Havana City, Cuba

    Roberto Rodríguez-Labrada & Yaimee Vázquez-Mojena

  7. Reynosa-Aztlan Multidisciplinary Unit, Autonomous University of Tamaulipas, Fuente de Diana, Aztlán, 88740, Tamaulipas, Mexico

    Sergio Montes

  8. Department of Special Education, University of the Americas Mexico City College, Puebla # 223 Col. Roma Alcaldía Cuauhtemoc, 06700, Mexico City, Mexico

    Rigoberto González-Piña

Authors
  1. Laura E. Ramos-Languren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alberto Avila-Luna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriela García-Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roberto Rodríguez-Labrada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yaimee Vázquez-Mojena
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carmen Parra-Cid
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sergio Montes
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Antonio Bueno-Nava
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rigoberto González-Piña
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RG-P, LER-L and AB-N participated in the conceptualization of this study and the development of the aim, analyzed and interpreted the data and contributed to the writing of this manuscript. AA-L, GG-D and SM carried out the amino acid measurements by HPLC and contributed to the writing of this manuscript. CP-C participated in the conceptualization of the study, performed the histological interpretation and contributed to the writing of this manuscript. RR-L and YV-M performed the statistical analysis and interpretation of data and contributed to the writing of this manuscript. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Rigoberto González-Piña.

Ethics declarations

Conflict of interest

The authors do so declare that there are no conflicts of interest. The authors have no relevant financial or nonfinancial interests to disclose.

Ethical Approval

Approval was obtained from the Research Committee of the National Rehabilitation Institute LGII (Protocol No. 91/17). We adhered to the Guide for the Care and Use of Experimental Animals and the local regulation (Mexican regulation NOM-062-ZOO-1999).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramos-Languren, L.E., Avila-Luna, A., García-Díaz, G. et al. Glutamate, Glutamine, GABA and Oxidative Products in the Pons Following Cortical Injury and Their Role in Motor Functional Recovery. Neurochem Res 46, 3179–3189 (2021). https://doi.org/10.1007/s11064-021-03417-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-021-03417-8

Keywords

Search

Navigation