Possible role of GABAergic depolarization in neocortical neurons in generating hyperexcitatory behaviors during emergence from sevoflurane anesthesia in the rat

ASN Neuro

Volumn 6, Issue 2, 2014, Pages 127-136

  Lim, Byung Gun ^a   Shen, Feng Yan ^a,b   Kim, Young Beom ^a   Kim, Woong Bin ^a   Kim, Yoon Sik ^a   Han, Hee Chul ^a   Lee, Mi Kyoung ^a   Kong, Myoung Hoon ^a   Kim, Yang In ^a  

^a Korea University College of Medicine   (South Korea)

^b XINHUA HOSPITAL AFFILIATED TO SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Emergence agitation; GABA; KCC2; Neocortex; NKCC1; Sevoflurane

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BUMETANIDE; SEVOFLURANE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ETHER DERIVATIVE; INHALATION ANESTHETIC AGENT; INTRAVENOUS ANESTHETIC AGENT; LOOP DIURETIC AGENT; PROPOFOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BILATERAL FORELIMB OR HINDLIMB; BLOOD GAS; BRAIN CORTEX; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EVOKED RESPONSE; EXPERIMENTAL BEHAVIORAL TEST; GABAERGIC SYSTEM; GAS CHROMATOGRAPHY; HEAD SHAKING; HYPEREXCITATORY BEHAVIOR; MALE; NONHUMAN; PH MEASUREMENT; POSTSYNAPTIC POTENTIAL; RAT; RESPIRATION DEPRESSION; SEIZURE; SIDE TO SIDE ROLLING; TREMBLING; UNILATERAL FORELIMB OR HINDLIMB; WANDERING; AGE; AKATHISIA; ANIMAL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MEMBRANE POTENTIAL; METABOLISM; NEOCORTEX; NERVE CELL; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPTIC POTENTIAL;

AGE FACTORS; AKATHISIA, DRUG-INDUCED; ANESTHETICS, INHALATION; ANESTHETICS, INTRAVENOUS; ANIMALS; BUMETANIDE; GAMMA-AMINOBUTYRIC ACID; MEMBRANE POTENTIALS; METHYL ETHERS; NEOCORTEX; NEURONS; PATCH-CLAMP TECHNIQUES; PROPOFOL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; SYNAPTIC POTENTIALS;

EID: 84901920964     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20140004     Document Type: Article

References (49)

1. Aono J, Ueda W, Mamiya K, Takimoto E, Manabe M (1997) Greater incidence of delirium during recovery from sevoflurane anesthesia in preschool boys. Anesthesiology 87:1298-1300.
2. Aouad MT, Yazbeck-Karam VG, Nasr VG, El-Khatib MF, Kanazi GE, Bleik JH (2007) A single dose of propofol at the end of surgery for the prevention of emergence agitation in children undergoing strabismus surgery during sevoflurane anesthesia. Anesthesiology 107:733-738.
3. Baccei ML, Fitzgerald M (2004) Development of GABAergic and glycinergic transmission in the neonatal rat dorsal horn. J Neurosci 24:4749-4757.
4. Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
5. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87:1215-1284.
6. Bough KJ, Gudi K, Han FT, Rathod AH, Eagles DA (2002) An anticonvulsant profile of the ketogenic diet in the rat. Epilepsy Res 50:313-325.
7. Brailowsky S, Kunimoto M, Menini C, Silva-Barrat C, Riche D, Naquet R (1988) The GABA-withdrawal syndrome: a new model of focal epileptogenesis. Brain Res 442:175-179.
8. Brandt C, Nozadze M, Heuchert N, Rattka M, Loscher W (2010) Disease-modifying effects of phenobarbital and the NKCC1 inhibitor bumetanide in the pilocarpine model of temporal lobe epilepsy. J Neurosci 30:8602-8612.
9. Breschan C, Platzer M, Jost R, Stettner H, Likar R (2007) Midazolam does not reduce emergence delirium after sevoflurane anesthesia in children. Paediatr Anaesth 17:347-352.
10. Bryan YF, Hoke LK, Taghon TA, Nick TG, Wang Y, Kennedy SM, Furstein JS, Kurth CD (2009) A randomized trial comparing sevoflurane and propofol in children undergoing MRI scans. Paediatr Anaesth 19:672-681.
11. Choi HJ, Lee CJ, Schroeder A, Kim YS, Jung SH, Kim JS, Kim do Y, Son EJ, Han HC, Hong SK, Colwell CS, Kim YI (2008) Excitatory actions of GABA in the suprachiasmatic nucleus. J Neurosci 28:5450-5459.
12. Cleary RT, Sun H, Huynh T, Manning SM, Li Y, Rotenberg A, Talos DM, Kahle KT, Jackson M, Rakhade SN, Berry G, Jensen FE (2013) Bumetanide enhances phenobarbital efficacy in a rat model of hypoxic neonatal seizures. PLoS ONE 8:e57148.
13. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421.
14. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, De Koninck P, De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424:938-942.
15. Dahmani S, Stany I, Brasher C, Lejeune C, Bruneau B, Wood C, Nivoche Y, Constant I, Murat I (2010) Pharmacological prevention of sevofluraneand desflurane-related emergence agitation in children: a meta-analysis of published studies. Br J Anaesth 104:216-223.
16. DeFazio RA, Heger S, Ojeda SR, Moenter SM (2002) Activation of A-type gamma-aminobutyric acid receptors excites gonadotropin-releasing hormone neurons. Mol Endocrinol 16:2872-2891.
17. Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ (2005) NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11:1205-1213.
18. Edwards DA, Shah HP, Cao W, Gravenstein N, Seubert CN, Martynyuk AE (2010) Bumetanide alleviates epileptogenic and neurotoxic effects of sevoflurane in neonatal rat brain. Anesthesiology 112:567-575.
19. Farthing D, Gehr L, Berger B, Fakhry I, Sica D (1997) Simple method for simultaneous determination of halothane, enflurane, and isoflurane in Krebs solution using capillary gas chromatography. Biomed Chromatogr 11:29-32.
20. Franks NP, Lieb WR (1996) Temperature dependence of the potency of volatile general anesthetics: implications for in vitro experiments. Anesthesiology 84:716-720.
21. Haam J, Popescu IR, Morton LA, Halmos KC, Teruyama R, Ueta Y, Tasker JG (2012) GABA is excitatory in adult vasopressinergic neuroendocrine cells. J Neurosci 32:572-582.
22. He Q, Nomura T, Xu J, Contractor A (2014) The developmental switch in GABA polarity is delayed in fragile X mice. J Neurosci 34:446-450.
23. Jerome EH (1989) Recovery of the pediatric patient from anesthesia. In: Pediatric Anesthesia, 2nd edn. (Gregory GA, ed.), p. 629, New York: Churchill Livingstone.
24. Kanaya A, Kuratani N, Satoh D, Kurosawa S (2014) Lower incidence of emergence agitation in children after propofol anesthesia compared with sevoflurane: a meta-analysis of randomized controlled trials. J Anesth. 28:4-11.
25. Kim DY, Choi HJ, Kim JS, Kim YS, Jeong DU, Shin HC, Kim MJ, Han HC, Hong SK, Kim YI (2005) Voltage-gated calcium channels play crucial roles in the glutamate-induced phase shifts of the rat suprachiasmatic circadian clock. Eur J Neurosci 21:1215-1222.
26. Kim JS, Kim WB, Kim YB, Lee Y, Kim YS, Shen FY, Lee SW, Park D, Choi HJ, Hur J, Park JJ, Han HC, Colwell CS, Cho YW, Kim YI (2011a) Chronic hyperosmotic stress converts GABAergic inhibition into excitation in vasopressin and oxytocin neurons in the rat. J Neurosci 31:13312-13322.
27. Kim YB, Kim YS, Kim WB, Shen FY, Lee SW, Chung HJ, Kim JS, Han HC, Colwell CS, Kim YI (2013) GABAergic excitation of vasopressin neurons: possible mechanism underlying sodium-dependent hypertension. Circ Res 113:1296-1307.
28. Kim YH, Yoon SZ, Lim HJ, Yoon SM (2011b) Prophylactic use of midazolam or propofol at the end of surgery may reduce the incidence of emergence agitation after sevoflurane anaesthesia. Anaesth Intensive Care 39:904-908.
29. Ko YP, Huang CJ, Hung YC, Su NY, Tsai PS, Chen CC, Cheng CR (2001) Premedication with low-dose oral midazolam reduces the incidence and severity of emergence agitation in pediatric patients following sevoflurane anesthesia. Acta Anaesthesiol Sin 39:169-177.
30. Murase K, Ryu PD, Randic M (1989) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 103:56-63.
31. Nakane R, Oka Y (2010) Excitatory action of GABA in the terminal nerve gonadotropin-releasing hormone neurons. J Neurophysiol 103:1375-1384.
32. Nakayama S, Furukawa H, Yanai H (2007) Propofol reduces the incidence of emergence agitation in preschool-aged children as well as in school-aged children: a comparison with sevoflurane. J Anesth 21:19-23.
33. Newman J (1995) Thalamic contributions to attention and consciousness. Conscious Cogn 4:172-193.
34. Olympio MA (1991) Postanesthetic delirium: historical perspectives. J Clin Anesth 3:60-63.
35. Owens DF, Boyce LH, Davis MB, Kriegstein AR (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16:6414-6423.
36. Payne JA, Rivera C, Voipio J, Kaila K (2003) Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26:199-206.
37. Pedersen NA, Jensen AG, Kilmose L, Olsen KS (2013) Propofol-remifentanil or sevoflurane for children undergoing magnetic resonance imaging? A randomised study. Acta Anaesthesiol Scand 57:988-995.
38. Plotkin MD, Snyder EY, Hebert SC, Delpire E (1997) Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain. J Neurobiol 33:781-795.
39. Rheims S, Minlebaev M, Ivanov A, Represa A, Khazipov R, Holmes GL, Ben-Ari Y, Zilberter Y (2008) Excitatory GABA in rodent developing neocortexin vitro. J Neurophysiol 100:609-619.
40. Russell JM (2000) Sodium-potassium-chloride cotransport. Physiol Rev 80:211-276.
41. Schiff ND (2008) Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Ann N Y Acad Sci 1129:105-118.
42. Szabadics J, Varga C, Molnar G, Olah S, Barzo P, Tamas G (2006) Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311:233-235.
43. Viitanen H, Annila P, Viitanen M, Tarkkila P (1999) Premedication with midazolam delays recovery after ambulatory sevoflurane anesthesia in children. Anesth Analg 89:75-79.
44. Vlajkovic GP, Sindjelic RP (2007) Emergence delirium in children: many questions, few answers. Anesth Analg 104:84-91.
45. Wells LT, Rasch DK (1999) Emergence 'delirium' after sevoflurane anesthesia: a paranoid delusion? Anesth Analg 88:1308-1310.
46. Workman AD, Charvet CJ, Clancy B, Darlington RB, Finlay BL (2013) Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci 33:7368-7383.
47. Wu J, Harata N, Akaike N (1996) Potentiation by sevoflurane of the gamma-aminobutyric acid-induced chloride current in acutely dissociated CA1 pyramidal neurones from rat hippocampus. Br J Pharmacol 119:1013-1021.
48. Xu G, Broadbelt KG, Haynes RL, Folkerth RD, Borenstein NS, Belliveau RA, Trachtenberg FL, Volpe JJ, Kinney HC (2011) Late development of the GABAergic system in the human cerebral cortex and white matter. J Neuropathol Exp Neurol 70:841-858.
49. Yamada J, Okabe A, Toyoda H, Kilb W, Luhmann HJ, Fukuda A (2004) Cluptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557:829-841.