Experimental Brain Research

, Volume 214, Issue 3, pp 463–469 | Cite as

Potentiation of spontaneous and evoked cortical electrical activity after spreading depression: in vivo analysis in well-nourished and malnourished rats

  • Thays Kallyne Marinho de Souza
  • Mariana Barros e Silva
  • André Ricardson Gomes
  • Hélio Magalhães de Oliveira
  • Renato Barros Moraes
  • Catão Temístocles de Freitas Barbosa
  • Rubem Carlos Araújo Guedes
Research Article

Abstract

Cortical spreading depression (CSD) is influenced by brain excitability and is related to neurological diseases, such as epilepsy. In vitro evidence indicates that neuronal electrical activity is potentiated after CSD. Malnutrition can cause electrophysiological changes in the brain, both in animals and in humans. Here, we investigated in vivo whether CSD potentiates the amplitude of electrocorticogram (ECoG) and of transcallosal evoked responses in adult well-nourished (W), early-malnourished (M), and food-restricted rats. ECoG amplitudes were compared before and after CSD, at two parietal regions (designated the anterior and posterior regions). In the anterior region, post-CSD amplitudes of the ECoG waves were 13–23% higher (P < 0.05) than the pre-CSD values in all groups. In the posterior region, amplitudes increased 22% in the M group only (P < 0.05). In a fourth CSD-free group, ECoG amplitude did not change during the four recording hours. Transcallosal electrically evoked cortical responses also increased 21.5 ± 9.6% and 41.8 ± 28.5%, after CSD, in the W and M conditions, respectively, as compared to pre-CSD values. The data support the hypothesis of an in vivo CSD potentiation on cortical excitability as recorded by spontaneous and evoked electrical activity and modulation by nutritional status.

Keywords

Brain excitability Cerebral cortex EEG Rat Transcallosal responses 

References

  1. Almeida SS, Duntas LH, Dye L, Nunes ML, Prasad C, Rocha JBT, Wainwright P, Zaia CTBV, Guedes RCA (2002) Nutrition and brain function: a multidisciplinary virtual symposium. Nutr Neurosci 5:311–320PubMedCrossRefGoogle Scholar
  2. Anwyl R (2009) Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharmacology 56:735–740PubMedCrossRefGoogle Scholar
  3. Barret DE, Radke-Yarrow M (1985) Effects of nutritional supplementation on children’s responses to novel, frustrating and competitive situations. Am J Clin Nutr 42:102–120Google Scholar
  4. Berger M, Speckmann E-J, Pape HC, Gorji A (2008) Spreading depression enhances human neocortical excitability in vitro. Cephalalgia 28:558–562PubMedCrossRefGoogle Scholar
  5. Bernard J, Lahsaini A, Massicote G (1994) Potassium-induced long-term potentiation in area CA1 of the hippocampus involves phospholipase activation. Hippocampus 4:447–453PubMedCrossRefGoogle Scholar
  6. Bogdanov VB, Multon S, Chauvel V, Bogdanova OV, Prodanov D, Makarchuk MY, Schoenen J (2011) Migraine preventive drugs differentially affect cortical spreading depression in rat. Neurobiol Dis 41:430–435PubMedCrossRefGoogle Scholar
  7. Bruce EN (2000) Biomedical signal processing and signal modeling. Wiley, New YorkGoogle Scholar
  8. Cheetham CE, Finnerty GT (2007) Plasticity and its role in neurological diseases of the adult nervous system. Adv Clin Neurosci Rehabil 7:8–9PubMedGoogle Scholar
  9. Díaz-Cintra S, González-Maciel A, Ángel–Morales M, Aguilar A, Cintra L, Prado-Alcalá RA (2007) Protein malnutrition differentially alters the number of glutamic acid decarboxylase-67 interneurons in dentate gyrus and CA1–3 subfields of the dorsal hippocampus. Exp Neurol 208:47–53PubMedCrossRefGoogle Scholar
  10. Faraguna U, Nelson A, Vyazovskiy VV, Cirelli C, Tononi G (2010) Unilateral cortical spreading depression affects sleep need and induces molecular and electrophysiological signs of synaptic potentiation in vivo. Cereb Cortex 20:2939–2947PubMedCrossRefGoogle Scholar
  11. Feoli AM, Siqueira I, Almeida LMV, Tramontina AC, Battu C, Wofchuk ST, Gottfried C, Perry ML, Gonçalves CA (2006) Brain glutathione content and glutamate uptake are reduced in rats exposed to pre- and postnatal protein malnutrition. J Nutr 136:2357–2361PubMedGoogle Scholar
  12. Florian ML, Nunes ML (2010) Effects of intra-uterine and early extra-uterine malnutrition on seizure threshold and hippocampal morphometry of pup rats. Nutr Neurosci 13:265–273PubMedGoogle Scholar
  13. Footitt DR, Newberry NR (1998) Cortical spreading depression induces an LTP-like effect in rat neocortex in vitro. Brain Res 781:339–342Google Scholar
  14. Frazão MF, Maia LMSS, Guedes RCA (2008) Early malnutrition, but not age, modulates in the rat the l-arginine facilitating effect on cortical spreading depression. Neurosci Lett 447:26–30PubMedCrossRefGoogle Scholar
  15. Goadsby PJ (2006) Recent advances in understanding migraine mechanisms, molecules and Therapeutics. Trends in Mol Med 13:39–44CrossRefGoogle Scholar
  16. Gorji A, Speckmann E (2004) Spreading depression enhances the spontaneous epileptiform activity in human neocortical tissues. Europ J Neurosci 19:3371–3374CrossRefGoogle Scholar
  17. Gorji A, Zahn PK, Pogatzki EM, Speckmann E-J (2004) Spinal and cortical spreading depression enhance spinal cord activity. Neurobiol Dis 15:70–79PubMedCrossRefGoogle Scholar
  18. Grieve PG, Isler JR, Izraelit A, Peterson BS, Fifer WP, Myers MM, Stark RI (2008) EEG functional connectivity in term age extremely low birth weight infants. Clin Neurophysiol 119:2712–2720PubMedCrossRefGoogle Scholar
  19. Guedes RCA (2005) Electrophysiological methods: application in nutritional neuroscience. In: Lieberman H, Kanarek R, Prasad C (eds) Nutritional neuroscience, overview of an emerging field. CRC Press, New York, pp 39–44Google Scholar
  20. Guedes RCA, Cavalheiro EA (1997) Blockade of spreading depression in chronic epileptic rats: reversion by diazepam. Epil Res 27:33–40CrossRefGoogle Scholar
  21. Guedes RCA, Do Carmo RJ (1980) Influence of ionic alterations produced by gastric washing on cortical spreading depression. Exp Brain Res 39:341–349PubMedCrossRefGoogle Scholar
  22. Guedes RCA, Cabral-Filho JE, Teodósio NR (1992) GABAergic mechanisms involved in cortical spreading depression in normal and malnourished rats. In: Do Carmo RJ (ed) Spreading depression. Springer, Berlin, pp 17–26Google Scholar
  23. Guedes RCA, Tsurudome K, Matsumoto N (2005) Spreading depression in vivo potentiates electrically-driven responses in frog optic tectum. Brain Res 1036:109–114PubMedCrossRefGoogle Scholar
  24. Hack M, Breslau N, Weissman B, Aram D, Klein N, Borawski E (1991) Effects of very birth weight and subnormal head size on cognitive abilities at school age. New Engl J Med 325:321–327CrossRefGoogle Scholar
  25. Hadjikhani N, del Rio MS, Wu O, Schwartz D, Bakker D, Fischl B, Kwong KK, Cutrer FM, Rosen BR, Tootell RB, Sorensen AG, Moskowitz MA (2001) Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Neurobiol 98:4687–4692Google Scholar
  26. Hicks TP, Conti F (1996) Amino acids as the source of considerable excitation in cerebral cortex. Can J Physiol Pharmacol 74:341–361PubMedGoogle Scholar
  27. Izquierdo I, Cammarota M, Da Silva WC, Lia RM, Bevilaqua LR, Rossato JI, Bonini JS, Mello P, Benetti F, Costa JC, Medina JH (2008) The evidence for hippocampal long-term potentiation as a basis of memory for simple tasks. An Acad Brasil Ciênc 80:115–127PubMedGoogle Scholar
  28. Largo C, Ibarz JM, Herreras O (1997) Effects of the gliotoxin fluorocitrate on spreading depression and glial membrane potential in rat brain in situ. J Neurophysiol 78:295–307PubMedGoogle Scholar
  29. Leão AAP (1944) Spreading depression of activity in the cerebral cortex J Neurophysiol 7:359–390Google Scholar
  30. Leão AAP (1947) The slow voltage variation of spreading depression of activity. J Neurophysiol 10:409–414PubMedGoogle Scholar
  31. McMahon LL, Kauer JA (1997) Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18:295–305PubMedCrossRefGoogle Scholar
  32. Merkler D, Klinker F, Jürgens T, Glaser R, Paulus W, Brinkmann BG, Sereda M, Guedes RCA, Brück W, Liebetanz D (2009) Propagation of spreading depression inversely correlates with cortical myelin content. Ann Neurol 66:355–365PubMedCrossRefGoogle Scholar
  33. Miyazawa D, Yasui Y, Yamada K, Ohara N, Okuyama H (2010) Regional differences of the mouse brain in response to an α-linolenic acid-restricted diet: Neurotrophin content and protein kinase activity. Life Sci 87:490–494PubMedCrossRefGoogle Scholar
  34. Morgane PJ, Miller M, Kemper T, Stern W, Forbes W, Hall R, Bronzino J, Kissane J, Hawrylewicz E, Resnick O (1978) The effects of protein malnutrition on the developing nervous system in the rat. Neurosci Biobehav Rev 2:137–230CrossRefGoogle Scholar
  35. Morgane PJ, Mokler DJ, Galler JR (2002) Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 26:471–483PubMedCrossRefGoogle Scholar
  36. Moskowitz MA (2007) Pathophysiology of headache—past and present. Headache 47(Suppl 1):58–63CrossRefGoogle Scholar
  37. Picanço-Diniz CW, Araújo MS, Borba JMC, Guedes RCA (1998) NADPHdiaphorase containing neurons and biocytin-labelled axon terminals in the visual cortex of adult rats malnourished during development. Nutr Neurosci 1:35–48Google Scholar
  38. Plagemann A, Harder T, Rake A, Waas T, Melchior K, Ziska T, Rohde W, Dorner G (1999) Observations on the orexigenic hypothalamic neuropeptide Y system in neonatally overfed weanling rats. J Neuroendocrinol 11:541–546PubMedCrossRefGoogle Scholar
  39. Ranade SC, Rose A, Rao M, Gallego J, Gressens P, Mani S (2008) Many different types of nutritional deficiencies affect different domains of spatial memory function checked in a radial arm maze. Neurosci 152:859–866CrossRefGoogle Scholar
  40. Rich NJ, Van Landingham JW, Figueiroa S, Seth R, Corniola RS, Levenson CW (2010) Chronic caloric restriction reduces tissue damage and improves spatial memory in a rat model of traumatic brain injury. J Neurosci Res 88:2933–2939PubMedGoogle Scholar
  41. Rocha-de-Melo AP, Cavalcanti JB, Barros AS, Guedes RCA (2006) Manipulation of rat litter size during suckling influences cortical spreading depression after weaning and at adulthood. Nutr Neurosci 9:155–160PubMedCrossRefGoogle Scholar
  42. Sloan HL, Austin VC, Blamire AM, Schnupp JWH, Lowe AS, Allers KA, Matthews PM, Sibson NR (2010) Regional differences in neurovascular coupling in rat brain as determined by fMRI and electrophysiology. NeuroImage 53:399–411PubMedCrossRefGoogle Scholar
  43. Somjen GG, Aitken PG, Czeh GL, Herrera O, Jing J, Young JN (1992) Mechanism of spreading depression: a review of recent findings and a hypothesis. Can J Physiol Pharmacol 70:248–254CrossRefGoogle Scholar
  44. Soto-Moyano R, Fernandez V, Sanhueza M, Belmar J, Kusch C, Perez H, Ruiz S, Hernandez A (1999) Effects of mild protein prenatal malnutrition and subsequent postnatal nutritional rehabilitation on noradrenaline release and neuronal density in the rat occipital cortex. Dev Brain Res 116:51–58CrossRefGoogle Scholar
  45. Strupp BJ, Levitsky DA (1995) Enduring cognitive effects of early malnutrition: a theoretical reappraisal. J Nutr 125:2221–2232Google Scholar
  46. Wolff GL, Kodell RL, Kaput JA (1999) Caloric restriction abolishes enhanced metabolic efficiency induced by ectopic agouti protein in yellow mice. Proc Soc Exp Biol Med 221:99–104PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Thays Kallyne Marinho de Souza
    • 1
  • Mariana Barros e Silva
    • 1
  • André Ricardson Gomes
    • 2
  • Hélio Magalhães de Oliveira
    • 2
  • Renato Barros Moraes
    • 3
  • Catão Temístocles de Freitas Barbosa
    • 3
  • Rubem Carlos Araújo Guedes
    • 1
  1. 1.Departamento de NutriçãoUniversidade Federal de PernambucoRecifeBrazil
  2. 2.Departamento de Eletrônica e SistemasUniversidade Federal PernambucoRecifeBrazil
  3. 3.Universidade Federal Rural de PernambucoRecifeBrazil

Personalised recommendations