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Electron microscopic GABA evaluation in hippocampal mossy terminals of genetic absence epilepsy rats receiving kindling stimulations

Year 2022, , 981 - 987, 30.12.2022

Nuray Nükhet İmdat , Özlem Tuğçe Çilingir-kaya , Zehra Nur Turgan âşık Tuğba Karamahmutoğlu Medine Gülçebi İdriz Oğlu , Dilek Akakın , Filiz Onat , Serap Şirvancı

https://doi.org/10.33808/clinexphealthsci.1030132

Abstract

Objective: The hypotheses related to the fact of epileptic mechanisms are mainly based on excitation-inhibition imbalance in central nervous system. GAERS (Genetic Absence Epilepsy Rats from Strasbourg) is a well-known animal model of absence epilepsy, and frequently used in experimental studies. In the present study, we aimed to examine possible morphological and gamma-aminobutyric acid (GABA) density changes in GAERS hippocampus after electrical kindling stimulations.
Methods: All control and test group rats received 6 kindling stimulations. Rats were decapitated 1 h after the last stimulation. Ultrastructural GABA immunocytochemistry was used to evaluate GABA density quantitatively in mossy terminals of hippocampal CA3 region.
Results: GABA levels were less in kindling groups compared to their controls, and in GAERS groups compared to Wistar groups; mitochondrial and dendritic spine area ratios were greater in GAERS groups compared to Wistar groups, although all these evaluations were statistically nonsignificant. Depletion of synaptic vesicles was evident in the mossy terminals of kindling groups.
Conclusion: The reason of decreased levels of GABA found in the present study might be that GABA has been released from the synaptic pool rapidly at an early time period after the last stimulation, for compansation mechanisms. Depletion of synaptic vesicles observed in kindling groups shows that even 6 kindling stimulations have an impact of changing hippocampal morphology in trisynaptic cycle. The increased mitochondrial area in GAERS might be related to the increased mitochondrial activity. The increased dendritic spine area might be related to the increased performance of learning in GAERS. Our findings indicating that absence epilepsy and temporal lobe epilepsy have different mechanisms of epileptogenesis might be a basis for further experimental studies

Keywords

Absence epilepsy GAERS hippocampus kindling GABA immunocytochemistry

References

  • [1] Bambal G, Çakıl D, Ekici F. Deneysel epilepsi modelleri. J Clin Exp Invest 2011;2(1):118-123. (Turkish)
  • [2] Zupec-Kania BA, Spellman E. An overview of the ketogenic diet for pediatric epilepsy. Nutr Clin Pract 2009;23(6):589-596.
  • [3] Jehaa LE, Morris HH, Burgess RC. Coexistence of focal and idiopathic generalized epilepsy in the same patient population. Seizure 2006;15(1):28-34.
  • [4] Koutroumanidis M, Hennessy M, Elwes RD. Coexistence of temporal lobe and idiopathic generalized epilepsies. Neurology 1999;53(3):490-495.
  • [5] Eskazan E, Onat FY, Aker R, Oner G. Resistance to propagation of amygdaloid kindling seizures in rats with genetic absence epilepsy. Epilepsia 2002;43(10):1115-1119.
  • [6] Sandler R, Smith AD. Coexistence of GABA and glutamate in mossy fiber terminals of the primate hippocampus: an ultrastructural study. J Comp Neurol 1991;303(2):177-192.
  • [7] Schwarzer C, Sperk G. Hippocampal granule cells Express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 1995;69(3):705-709.
  • [8] Avanzini G, Panzica F, de Curtis M. The role of the thalamus in vigilance and epileptogenic mechanisms. Clin Neurophysiol 2000;111(Suppl 2:S):19-26.
  • [9] Liu Z, Mikati M, Holmes GL. Mesial temporal sclerosis: pathogenesis and significance. Pediatr Neurol 1995;12(1):5- 16.
  • [10] Marescaux C, Vergnes M. Genetic absence epilepsy in rats from Strasbourg (GAERS). Ital J Neurol Sci 1995;16(1-2):113- 118.
  • [11] Nehlig A, Vergnes M, Boyet S, Marescaux C. Local cerebral glucose utilization in adult and immature GAERS. Epilepsy Res 1998;32(1-2):206-212.
  • [12] Nehlig A, Vergnes M, Marescaux C, Boyet S. Mapping of cerebral energy metabolism in rats with genetic generalized nonconvulsive epilepsy. J Neural Transm 1992;35:141-153.
  • [13] Richards DA, Morrone LA, Bowery NG. Hippocampal extracellular amino acids and EEG spectral analysis in a genetic rat model of absence epilepsy. Neuropharmacology 2000;39(12):2433-2441.
  • [14] Vergnes M, Boehrer A, Reibel S, Simler S, Marescaux C. Selective susceptibility to inhibitors of GABA synthesis and antagonists of GABA-A receptor in rats with genetic absence epilepsy. Exp Neurol 2000;161(2):714-723.
  • [15] Brailowsky ST, Montiel A, Boehrer C, Marescaux, Vergnes M. Susceptibility to focal and generalized seizures in Wistar rats with genetic absence-like epilepsy. Neuroscience 1999;93(3):1173-1177.
  • [16] Gloor P, Fariello RG. Generalized epilepsy: some of its cellular mechanisms differ from those of focal epilepsy. Trends Neurosci 1988;11(2):63-68.
  • [17] Vergnes M, Marescaux C. Pathophysiological mechanisms underlying genetic absence epilepsy in rats. In: Idiopathic generalized epilepsies: Clinical, experimental and genetic aspects (Malafosse A, Hirsch E, Marescaux C, Broglin D, Bernasconi R, Eds.). 1994; pp. 151-168, Libbey, London.
  • [18] Fromm GH. Role of inhibitory mechanisms in staring spells. J Clin Neurophysiol 1986;3(4):297-311.
  • [19] Myslobodsky MS. Petit mal epilepsy: Too little or too much GABA? In: Neurotransmitters, seizures, and epilepsy II (Fariello RG et al., Eds.), 1984; pp. 337-345, Raven Press, New York.
  • [20] Racine RJ. Modification of seizure activity by electrical stimulation. I. After-discharge threshold. Electroencephalogr Clin Neurophysiol 1972a;32(3):269-279.
  • [21] Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972b;32(3):281-294.
  • [22] Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF. Synaptic reorganisation by mossy fibers in human epileptic fascia dentata. Neuroscience 1991;42(2):351-363.
  • [23] Sirvanci S, Meshul CK, Onat F, San T. Immunocytochemical analysis of glutamate and GABA in hippocampus of genetic absence epilepsy rats (GAERS). Brain Res 2003;988(1-2):180- 188.
  • [24] Akakın D, Sirvancı S, Gurbanova A, Aker R, Onat F, San T. Ultrastructural GABA immunocytochemistry in the mossy fiber terminals of Wistar and genetic absence epileptic rats receiving amygdaloid kindling stimulations. Brain Res 2011;Mar 4:101- 108.
  • [25] Pierce JP, Milner TA. Parallel increases in the synaptic and surface areas of mossy fiber terminals following seizure induction. Synapse 2001; 39(3):249-256.
  • [26] Hillman DE, Chen S. Reciprocal relationship between size of postsynaptic densities and their number: constancy in contact area. Brain Res 1984;295(2):325-343.
  • [27] Hillman DE, Chen S. Compensation in the number of presynaptic dense projections and synaptic vesicles in remaining parallel fibres following cerebellar lesions. J Neurocytol 1985;14(4):673-687.
  • [28] Olney JW. Glutamate-induced neuronal necrosis in the infant mouse hypothalamus: an electron microscopic study. J Neuropathol Exp Neurol 1971;30(1):75-90.
  • [29] Olney JW, Rhee V, Ho OL. Kainic acid: a powerful neurotoxic analogue of flutamate. Brain Res 1974;77(3):507-512.
  • [30] Sirvanci S, Meshul CK, Onat F, San T. Glutamate and GABA immunocytochemical electron microscopy in the hippocampal dentate gyrus of normal and genetic absence epilepsy rats. Brain Res 2005;16;1053(1-2):108-115.
  • [31] Acsady L, Kamondi A, Sık A, Freund T, Buzsaki G. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippcoampus. J Neurosci 1998;18(9):3386-3403.
  • [32] Claiborne BJ, Amaral DG, Cowan WM. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J. Comp Neurol 1986;246(4):435-458.
  • [33] Frotscher M. Mossy fibres from synapses with identified pyramidal basket cells in the CA3 region of the guinea-pig hippocampus: a combined Golgi-electron microscope study. J Neurocytol 1985;14(2):245-259.
  • [34] Soriano E, Frotscher M. Spiny nonpyramidal neurons in the CA3 region of the rat hippocampus are glutamate-like immunoreactive and receive convergent mossy fiber input. J Comp Neurol 1993;333(3):435-448.
  • [35] Sirvanci S, Canillioglu Y, Akakin D, Midillioglu S, Yildiz SD, Onat F, San T. Glutamic acid decarboxylase immunoreactivity in the mossy fiber terminals of the hippocampus of genetic absence epileptic rats. Turkish Neurosurg 2011;21(4):499-503.
  • [36] Meshul CK, Stallbaumer RK, Taylor B, Janowsky A. Haloperidol induced synaptic changes in striatum are associated with glutamate synapses. Brain Res 1994;648(2):181-195.
  • [37] Fiala JC, Spacek J, Harris KM. Dendritic spine pathology: Cause or consequence of neurological disorders? Brain Res Rev 2002;39(1):29-54.
  • [38] Kaufmann WE, Moser HW. Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 2000;10(10):981-991.
  • [39] Üzüm G. Epileptik nöbet oluşumunda hücresel mekanizmalar. İstanbul Tıp Fakültesi Mecmuası 1998;61(4):512-516.
  • [40] Sirvanci S, Midillioglu S, Meshul CK, Onat F, San T. Dendritic spines in the hippocampus of genetic absence epilepsy rats (GAERS): an ultrastructural quantitative analysis. Marmara Medical Journal 2003;16(3):195-200.
  • [41] Drakew A, Müller M, Gahwiler BH, Thompson SM, Frotscher M. Spine loss in experimental epilepsy: quantitative light and electron microscopic analysis of intracellularly stained CA3 pyramidal cells in hippocampal slice cultures. Neuroscience 1996;70(1):31-45.
  • [42] Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 1992;99(2):195-231.
  • [43] Vergnes M, Marescaux C, Boehrer A, Depaulis A. Are rats with genetic absence epilepsy behaviorally impaired? Epilepsy Res 1991;9(2):97-104.
  • [44] Getova D, Bowerya NG. Effects of GABAB receptor antagonists on learning and memory retention in a rat model of absence epilepsy. Eur J Pharmacol 1997;320(1):9-13.
  • [45] Melø TM, Sonnewald U, Touret M, Nehlig A. Cortical glutamate metabolism is enhanced in a genetic model of absence epilepsy. J Cereb Blood Flow Metab 2006;26(12):1496-1506.
  • [46] Snead OC, Hosey LC. Exacerbation of seizures in children by carbamazepine. N Engl J Med 1985;313(15):916-921.
  • [47] Nehlig A, Vergnes M, Marescaux C, Boyet S, Lannes B. Local cerebral glucose utilization in rats with petit mal-like seizures. Ann Neurol 1991;29(1):72-77.
  • [48] Farias PA, Low SQ, Peterson GM, Ribak CE. Morphological evidence for altered synaptic organization and structure in the hippocampal formation of seizure-sensitive gerbils. Hippocampus 1992;2(3):229-245

Year 2022, , 981 - 987, 30.12.2022

Nuray Nükhet İmdat , Özlem Tuğçe Çilingir-kaya , Zehra Nur Turgan âşık Tuğba Karamahmutoğlu Medine Gülçebi İdriz Oğlu , Dilek Akakın , Filiz Onat , Serap Şirvancı

https://doi.org/10.33808/clinexphealthsci.1030132

Abstract

References

  • [1] Bambal G, Çakıl D, Ekici F. Deneysel epilepsi modelleri. J Clin Exp Invest 2011;2(1):118-123. (Turkish)
  • [2] Zupec-Kania BA, Spellman E. An overview of the ketogenic diet for pediatric epilepsy. Nutr Clin Pract 2009;23(6):589-596.
  • [3] Jehaa LE, Morris HH, Burgess RC. Coexistence of focal and idiopathic generalized epilepsy in the same patient population. Seizure 2006;15(1):28-34.
  • [4] Koutroumanidis M, Hennessy M, Elwes RD. Coexistence of temporal lobe and idiopathic generalized epilepsies. Neurology 1999;53(3):490-495.
  • [5] Eskazan E, Onat FY, Aker R, Oner G. Resistance to propagation of amygdaloid kindling seizures in rats with genetic absence epilepsy. Epilepsia 2002;43(10):1115-1119.
  • [6] Sandler R, Smith AD. Coexistence of GABA and glutamate in mossy fiber terminals of the primate hippocampus: an ultrastructural study. J Comp Neurol 1991;303(2):177-192.
  • [7] Schwarzer C, Sperk G. Hippocampal granule cells Express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 1995;69(3):705-709.
  • [8] Avanzini G, Panzica F, de Curtis M. The role of the thalamus in vigilance and epileptogenic mechanisms. Clin Neurophysiol 2000;111(Suppl 2:S):19-26.
  • [9] Liu Z, Mikati M, Holmes GL. Mesial temporal sclerosis: pathogenesis and significance. Pediatr Neurol 1995;12(1):5- 16.
  • [10] Marescaux C, Vergnes M. Genetic absence epilepsy in rats from Strasbourg (GAERS). Ital J Neurol Sci 1995;16(1-2):113- 118.
  • [11] Nehlig A, Vergnes M, Boyet S, Marescaux C. Local cerebral glucose utilization in adult and immature GAERS. Epilepsy Res 1998;32(1-2):206-212.
  • [12] Nehlig A, Vergnes M, Marescaux C, Boyet S. Mapping of cerebral energy metabolism in rats with genetic generalized nonconvulsive epilepsy. J Neural Transm 1992;35:141-153.
  • [13] Richards DA, Morrone LA, Bowery NG. Hippocampal extracellular amino acids and EEG spectral analysis in a genetic rat model of absence epilepsy. Neuropharmacology 2000;39(12):2433-2441.
  • [14] Vergnes M, Boehrer A, Reibel S, Simler S, Marescaux C. Selective susceptibility to inhibitors of GABA synthesis and antagonists of GABA-A receptor in rats with genetic absence epilepsy. Exp Neurol 2000;161(2):714-723.
  • [15] Brailowsky ST, Montiel A, Boehrer C, Marescaux, Vergnes M. Susceptibility to focal and generalized seizures in Wistar rats with genetic absence-like epilepsy. Neuroscience 1999;93(3):1173-1177.
  • [16] Gloor P, Fariello RG. Generalized epilepsy: some of its cellular mechanisms differ from those of focal epilepsy. Trends Neurosci 1988;11(2):63-68.
  • [17] Vergnes M, Marescaux C. Pathophysiological mechanisms underlying genetic absence epilepsy in rats. In: Idiopathic generalized epilepsies: Clinical, experimental and genetic aspects (Malafosse A, Hirsch E, Marescaux C, Broglin D, Bernasconi R, Eds.). 1994; pp. 151-168, Libbey, London.
  • [18] Fromm GH. Role of inhibitory mechanisms in staring spells. J Clin Neurophysiol 1986;3(4):297-311.
  • [19] Myslobodsky MS. Petit mal epilepsy: Too little or too much GABA? In: Neurotransmitters, seizures, and epilepsy II (Fariello RG et al., Eds.), 1984; pp. 337-345, Raven Press, New York.
  • [20] Racine RJ. Modification of seizure activity by electrical stimulation. I. After-discharge threshold. Electroencephalogr Clin Neurophysiol 1972a;32(3):269-279.
  • [21] Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972b;32(3):281-294.
  • [22] Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF. Synaptic reorganisation by mossy fibers in human epileptic fascia dentata. Neuroscience 1991;42(2):351-363.
  • [23] Sirvanci S, Meshul CK, Onat F, San T. Immunocytochemical analysis of glutamate and GABA in hippocampus of genetic absence epilepsy rats (GAERS). Brain Res 2003;988(1-2):180- 188.
  • [24] Akakın D, Sirvancı S, Gurbanova A, Aker R, Onat F, San T. Ultrastructural GABA immunocytochemistry in the mossy fiber terminals of Wistar and genetic absence epileptic rats receiving amygdaloid kindling stimulations. Brain Res 2011;Mar 4:101- 108.
  • [25] Pierce JP, Milner TA. Parallel increases in the synaptic and surface areas of mossy fiber terminals following seizure induction. Synapse 2001; 39(3):249-256.
  • [26] Hillman DE, Chen S. Reciprocal relationship between size of postsynaptic densities and their number: constancy in contact area. Brain Res 1984;295(2):325-343.
  • [27] Hillman DE, Chen S. Compensation in the number of presynaptic dense projections and synaptic vesicles in remaining parallel fibres following cerebellar lesions. J Neurocytol 1985;14(4):673-687.
  • [28] Olney JW. Glutamate-induced neuronal necrosis in the infant mouse hypothalamus: an electron microscopic study. J Neuropathol Exp Neurol 1971;30(1):75-90.
  • [29] Olney JW, Rhee V, Ho OL. Kainic acid: a powerful neurotoxic analogue of flutamate. Brain Res 1974;77(3):507-512.
  • [30] Sirvanci S, Meshul CK, Onat F, San T. Glutamate and GABA immunocytochemical electron microscopy in the hippocampal dentate gyrus of normal and genetic absence epilepsy rats. Brain Res 2005;16;1053(1-2):108-115.
  • [31] Acsady L, Kamondi A, Sık A, Freund T, Buzsaki G. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippcoampus. J Neurosci 1998;18(9):3386-3403.
  • [32] Claiborne BJ, Amaral DG, Cowan WM. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J. Comp Neurol 1986;246(4):435-458.
  • [33] Frotscher M. Mossy fibres from synapses with identified pyramidal basket cells in the CA3 region of the guinea-pig hippocampus: a combined Golgi-electron microscope study. J Neurocytol 1985;14(2):245-259.
  • [34] Soriano E, Frotscher M. Spiny nonpyramidal neurons in the CA3 region of the rat hippocampus are glutamate-like immunoreactive and receive convergent mossy fiber input. J Comp Neurol 1993;333(3):435-448.
  • [35] Sirvanci S, Canillioglu Y, Akakin D, Midillioglu S, Yildiz SD, Onat F, San T. Glutamic acid decarboxylase immunoreactivity in the mossy fiber terminals of the hippocampus of genetic absence epileptic rats. Turkish Neurosurg 2011;21(4):499-503.
  • [36] Meshul CK, Stallbaumer RK, Taylor B, Janowsky A. Haloperidol induced synaptic changes in striatum are associated with glutamate synapses. Brain Res 1994;648(2):181-195.
  • [37] Fiala JC, Spacek J, Harris KM. Dendritic spine pathology: Cause or consequence of neurological disorders? Brain Res Rev 2002;39(1):29-54.
  • [38] Kaufmann WE, Moser HW. Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 2000;10(10):981-991.
  • [39] Üzüm G. Epileptik nöbet oluşumunda hücresel mekanizmalar. İstanbul Tıp Fakültesi Mecmuası 1998;61(4):512-516.
  • [40] Sirvanci S, Midillioglu S, Meshul CK, Onat F, San T. Dendritic spines in the hippocampus of genetic absence epilepsy rats (GAERS): an ultrastructural quantitative analysis. Marmara Medical Journal 2003;16(3):195-200.
  • [41] Drakew A, Müller M, Gahwiler BH, Thompson SM, Frotscher M. Spine loss in experimental epilepsy: quantitative light and electron microscopic analysis of intracellularly stained CA3 pyramidal cells in hippocampal slice cultures. Neuroscience 1996;70(1):31-45.
  • [42] Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 1992;99(2):195-231.
  • [43] Vergnes M, Marescaux C, Boehrer A, Depaulis A. Are rats with genetic absence epilepsy behaviorally impaired? Epilepsy Res 1991;9(2):97-104.
  • [44] Getova D, Bowerya NG. Effects of GABAB receptor antagonists on learning and memory retention in a rat model of absence epilepsy. Eur J Pharmacol 1997;320(1):9-13.
  • [45] Melø TM, Sonnewald U, Touret M, Nehlig A. Cortical glutamate metabolism is enhanced in a genetic model of absence epilepsy. J Cereb Blood Flow Metab 2006;26(12):1496-1506.
  • [46] Snead OC, Hosey LC. Exacerbation of seizures in children by carbamazepine. N Engl J Med 1985;313(15):916-921.
  • [47] Nehlig A, Vergnes M, Marescaux C, Boyet S, Lannes B. Local cerebral glucose utilization in rats with petit mal-like seizures. Ann Neurol 1991;29(1):72-77.
  • [48] Farias PA, Low SQ, Peterson GM, Ribak CE. Morphological evidence for altered synaptic organization and structure in the hippocampal formation of seizure-sensitive gerbils. Hippocampus 1992;2(3):229-245
There are 48 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Articles
Authors

Nuray Nükhet İmdat 0000-0003-1894-5320

Özlem Tuğçe Çilingir-kaya 0000-0002-2591-9174

Zehra Nur Turgan âşık This is me 0000-0002-2970-0495

Tuğba Karamahmutoğlu This is me 0000-0002-7025-2209

Medine Gülçebi İdriz Oğlu 0000-0003-4894-9867

Dilek Akakın 0000-0002-1781-3708

Filiz Onat 0000-0003-0680-4782

Serap Şirvancı 0000-0001-7683-4587

Publication Date December 30, 2022
Submission Date November 30, 2021
Published in Issue Year 2022

Cite

APA İmdat, N. N., Çilingir-kaya, Ö. T., Turgan âşık, Z. N., Karamahmutoğlu, T., et al. (2022). Electron microscopic GABA evaluation in hippocampal mossy terminals of genetic absence epilepsy rats receiving kindling stimulations. Clinical and Experimental Health Sciences, 12(4), 981-987. https://doi.org/10.33808/clinexphealthsci.1030132
AMA İmdat NN, Çilingir-kaya ÖT, Turgan âşık ZN, Karamahmutoğlu T, Gülçebi İdriz Oğlu M, Akakın D, Onat F, Şirvancı S. Electron microscopic GABA evaluation in hippocampal mossy terminals of genetic absence epilepsy rats receiving kindling stimulations. Clinical and Experimental Health Sciences. December 2022;12(4):981-987. doi:10.33808/clinexphealthsci.1030132
Chicago İmdat, Nuray Nükhet, Özlem Tuğçe Çilingir-kaya, Zehra Nur Turgan âşık, Tuğba Karamahmutoğlu, Medine Gülçebi İdriz Oğlu, Dilek Akakın, Filiz Onat, and Serap Şirvancı. “Electron Microscopic GABA Evaluation in Hippocampal Mossy Terminals of Genetic Absence Epilepsy Rats Receiving Kindling Stimulations”. Clinical and Experimental Health Sciences 12, no. 4 (December 2022): 981-87. https://doi.org/10.33808/clinexphealthsci.1030132.
EndNote İmdat NN, Çilingir-kaya ÖT, Turgan âşık ZN, Karamahmutoğlu T, Gülçebi İdriz Oğlu M, Akakın D, Onat F, Şirvancı S (December 1, 2022) Electron microscopic GABA evaluation in hippocampal mossy terminals of genetic absence epilepsy rats receiving kindling stimulations. Clinical and Experimental Health Sciences 12 4 981–987.
IEEE N. N. İmdat, Ö. T. Çilingir-kaya, Z. N. Turgan âşık, T. Karamahmutoğlu, M. Gülçebi İdriz Oğlu, D. Akakın, F. Onat, and S. Şirvancı, “Electron microscopic GABA evaluation in hippocampal mossy terminals of genetic absence epilepsy rats receiving kindling stimulations”, Clinical and Experimental Health Sciences, vol. 12, no. 4, pp. 981–987, 2022, doi: 10.33808/clinexphealthsci.1030132.
ISNAD İmdat, Nuray Nükhet et al. “Electron Microscopic GABA Evaluation in Hippocampal Mossy Terminals of Genetic Absence Epilepsy Rats Receiving Kindling Stimulations”. Clinical and Experimental Health Sciences 12/4 (December 2022), 981-987. https://doi.org/10.33808/clinexphealthsci.1030132.
JAMA İmdat NN, Çilingir-kaya ÖT, Turgan âşık ZN, Karamahmutoğlu T, Gülçebi İdriz Oğlu M, Akakın D, Onat F, Şirvancı S. Electron microscopic GABA evaluation in hippocampal mossy terminals of genetic absence epilepsy rats receiving kindling stimulations. Clinical and Experimental Health Sciences. 2022;12:981–987.
MLA İmdat, Nuray Nükhet et al. “Electron Microscopic GABA Evaluation in Hippocampal Mossy Terminals of Genetic Absence Epilepsy Rats Receiving Kindling Stimulations”. Clinical and Experimental Health Sciences, vol. 12, no. 4, 2022, pp. 981-7, doi:10.33808/clinexphealthsci.1030132.
Vancouver İmdat NN, Çilingir-kaya ÖT, Turgan âşık ZN, Karamahmutoğlu T, Gülçebi İdriz Oğlu M, Akakın D, Onat F, Şirvancı S. Electron microscopic GABA evaluation in hippocampal mossy terminals of genetic absence epilepsy rats receiving kindling stimulations. Clinical and Experimental Health Sciences. 2022;12(4):981-7.

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