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Year 2014, Volume: 27 Issue: 3, 171 - 177, 30.03.2015

Özlem Kirazlı Ümit Şehirli

https://doi.org/10.5472/MMJ.2014.03507.1

Abstract

Objective: Pedunculopontine nucleus (PPN) is a brainstem nucleus with an obscure border and located in the caudal tegmentum. In recent years, the numbers of studies related to PPN have been increasing due to its role in sleep/waking, in behavior, learning, and attention as well as its role in generation and control of locomotion. Besides cholinergic neurons, there are GABAergic, glutamatergic, dopaminergic and noradrenergic neurons in the PPN. Recently, the PPN has been a target for treatment of axial semptoms in Parkinson disease (PD). Calbindin, a member of the calcium binding protein family, which is an important molecule during protein synthesis has been related to neurodegenerative diseases. In our study, we investigated the developmental differences of calbindin expression which is related to GABAergic and glutamatergic neurons.Materials and Methods: The borders of the PPN were determined on the basis of the distribution of cholinergic neurons. Calbindin is expressed by GABAergic and glutamatergic neurons. Wistar rats aged 7, 14 and 21 days were perfused through the heart with a 4% paraformaldehyde solution. Brains were removed and 40 µm plane of sections were cut via microtome. Free-floating slices were stained with anti choline asetyltransferase and calbindin. In our study, we used 4 rats for each group, totally 12 rats were utilized. The number, location and diameters of calbindin positive neurons in PPN were evaluated in 7, 14 and 21 day-old rats.Results: The mean numbers of neurons were 30 ±3 at 7 days, 11 ±1 at 14 days and 150±50 at 21 days rats. There were statistically significant differences between 7 and 14 days and 14 and 21 day-old rats (p=0.0075 ve p=0.0343 respectively). The diameters of the neurons were 13 ±1.4 µm at 7 days, 11±1.6 µm at 14 days; 13.5±1.1µm at 21days. Conclusion: This study indicates that critical developmental changes in PPN occur between these intervals. These findings support and contribute to the findings of previous studies

Keywords

Tegmental pedunculopontine nucleus Calbindin GABAergic Cholinergic

References

  • 1. Garcia-Rill E. The pedunculopontine nucleus. Prog Neurobiol 1991; 36:363–89. doi:10.1016/0301-0082(91)90016-T
  • 2. Mena-Segovia J, Ross HM, Magill PJ, Bolam JP. The pedunculopontine nucleus: towards a functional integration with the basal ganglia. In: Bolam JP, Ingham JA, Magill PJ, editors. The Basal Ganglia VIII. Advances in Behavioral Biology. Volume 56. New York: Springer Science and Business Media, 2005:533-44.
  • 3. Pahapill PA, Lozano AM. The pedunculopontine nucleus and Parkinson’s disease. Brain 2000; 123:1767–83. doi: 10.1093/ brain/123.9.1767
  • 4. Pereira EA, Muthusamy KA, De Pennington N, Joint CA, Aziz TZ. Deep brain stimulation of the pedunculopontine nucleus in Parkinson’s disease. Preliminary experience at Oxford. Br J Neurosurg 2008; 22 Suppl 1:S41-4. doi:10.1080/02688690802448335.
  • 5. Mena-Segovia J, Micklem BR, Nair-Roberts RG, Ungless MA, Bolam JP. GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J Comp Neuro 2009; 515:397-408. doi: 10.1002/cne.22065.
  • 6. Semba K, Reiner PB, Fibiger HC. Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 1990; 38:643– 54. doi:10.1016/0306-4522(90)90058-C
  • 7. Semba K, Reiner PB, McGeer EG, Fibiger HC. Brainstem afferents to the magnocellular basal forebrain studied by axonal transport immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 1988; 267:433– 53.
  • 8. Lavoie B, Parent A. Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neuronsin the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 1994; 344:190–209.
  • 9. Clarke NP, Bevan MD, Cozzari C, Hartman BK, Bolam JP. Glutamate-enriched cholinergic synaptic terminals in the entopeduncular nucleus and subthalamic nucleus of the rat. Neuroscience 1997;2:371-85. doi:10.1016/S03064522(97) 00247-9
  • 10. Mena-Segovia J, Bolam JP, Magill PJ. Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family. Trends Neurosci 2004;10:585-8. doi:10.1016/ j.tins.2004.07.009
  • 11. Bolam JP, Francis CM, Henderson Z. Cholinergic input to dopaminergic neurons in the substantia nigra: a double immunocytochemical study. Neuroscience 1991;41:483-94.
  • 12. Garzon M, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM. Cholinergic axon terminals in the ventral tegmental area target a subpopulation of neurons expressing low levels of the dopamine transporter. J Comp Neurol 1999;410:197-210.
  • 13. Celio MR, Heizmann CW. Calcium-binding protein parvalbumin as a neuronal marker. Nature 1981;293:300-2.
  • 14. Baimbridge KG, Celio MR, Rogers JH. Calcium-binding proteins in the nervous system.Trends Neurosci 1992 ;15:303- 8.
  • 15. Härtig W, Brückner G, Brauer K, Seeger G, Bigl V. Triple immunofluorescence labelling of parvalbumin, calbindinD28k and calretinin in rat and monkey brain. J Neurosci Meth 1996 ;67:89-95.
  • 16. Lander ES, Linton LM, Birren B, NusbaumC, Zody MC, Baldwin J. Initial sequencing and analysis of the human genome. Nature 2001; 409:860–921.
  • 17. Celio MR. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 1990 ;35:375-475.
  • 18. Fortin M, Parent A. Calretinin-immunoreactive neurons in primate pedunculopontine and laterodorsal tegmental nuclei. Neuroscience 1999 ;88:535-47.
  • 19. Dun NJ, Dun SL, Hwang LL, Förstermann U. Infrequent co-existence of nitric oxide synthase and parvalbumin, calbindin and calretinin immunoreactivity in rat pontine neurons. Neurosci Lett 1995 26;191:165-8.
  • 20. Martinez-Gonzalez C, Micklem B R, Bolam JP, MenaSegovia J. Neurons containing calciumbinding proteins are topographically organized in the pedunculopontine nucleus. Program No. 845.17. 2009 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2009.
  • 21. Martinez-Gonzalez C, Bolam JP, Mena-Segovia J. Topographical organization of the pedunculopontine nucleus. Front Neuroanat 2011;5:22.
  • 22. Seto-Ohshima A, Emson PC, Lawson E, Mountjoy CQ, Carrasco LH. Loss of matrix calcium-binding proteincontaining neurons in Huntington’s disease. Lancet 1988; 1:1252-5.
  • 23. Côté PY, Parent A. Calbindin D-28k and choline acetyltransferase are expressed by different neuronal populations inpedunculopontine nucleus but not in nucleus basalis in squirrel monkeys Brain Res 1992 16;593:245-52.
  • 24. Tsuboi K, Kimber TA, Shults CW. Calretinin-containing axons and neurons are resistant to an intrastriatal 6-hydroxydopamine lesion. Brain Res 2000 ; 866:55-64.
  • 25. Bay KD, Mamiya K, Good CH, Skinner RD, Garcia-Rill E. Alpha-2 adrenergic regulation of pedunculopontine nucleus neurons during development. Neuroscience 2006; 141: 769–79.
  • 26. Simon C, Hayar A, Garcia-Rill E. Responses of developing pedunculopontine neurons to glutamate receptor agonists. J Neurophysiol 2011;105:1918-31. doi: 10.1152/jn.00953.2010.
  • 27. Jouvet-Mounier D, Astic L, Lacote D. Ontogenesis of thestates of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol 1970; 2: 216–39.
  • 28. Garcia-Rill E, Charlesworth A, Heister D, Ye M, Hayar A. The developmental decrease in REM sleep: the role of transmitters and electrical coupling. Sleep 2008;31:673-90.
  • 29. Thakkar M, Portas C, McCarley RW. Chronic low-amplitude electrical stimulation of the laterodorsal tegmental nucleus of freely moving cats increases REM sleep. Brain Res 1989; 723:223–27. doi:10.1016/0006-8993(96)00256-9
  • 30. Webster HH, Jones BE. Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in cat. II. Effects upon sleep-waking states. Brain Res 1988; 458:285–302. doi:10.1016/0006-8993(88)90471-4
  • 31. Steriade M, Datta S, Pare D, Oakson G, Curro Dossi R. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 1990; 10: 2541–59.
  • 32. Kobayashi T, Good C, Mamiya K, Skinner RD, Garcia-Rill E. Development of REM sleep drive and clinical implications. J Appl Physiol 2004; 96: 735–46. doi: 10.1152/japplphysiol. 00908.2003
  • 33. Kobayashi T, Good C, Biedermann J, Barnes C, Skinner RD, Garcia-Rill E. Developmental changes in pedunculopontine nucleus (PPN) neurons. J Neurophysiol 2004 ; 91:1470- 81. doi: 10.1152/jn.01024.2003
  • 34. Acsády L, Halasy K, Freund TF. Calretinin is present in nonpyramidal cells of the rat hippocampus--III. Their inputs from the median raphe and medial septal nuclei. Neuroscience 1993;52:829-41. doi:10.1016/0306-4522(93)90532-K
  • 35. Staiger JF, Masanneck C, Schleicher A, Zuschratter W. Calbindin containing interneurons are a target for VIPimmunoreactive synapses in rat primary somatosensory cortex. J Comp Neurol 2004;468:179-89. doi: 10.1002/cne.10953
  • 36. Parent M, Lévesque M, Parent A. Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J Comp Neurol 2001;439:162-75. doi: 10.1002/cne.1340
  • 37. Bhagwandin A, Gravett N, Bennett NC, Manger PR. Distribution of parvalbumin calbindin and calretinin containing neurons and terminal networks in relation to sleep associated nuclei in the brain of the giant Zambian mole-rat (Fukomys mechowii). J Chem Neuroanat 2013;52:69-79. doi: 10.1016/j.jchemneu.2013.06.002.

Nucleus pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel olarak incelenmesi

Year 2014, Volume: 27 Issue: 3, 171 - 177, 30.03.2015

Özlem Kirazlı Ümit Şehirli

https://doi.org/10.5472/MMJ.2014.03507.1

Abstract

Amaç: Kaudal tegmentumda yerleşimli, sınırları belirsiz bir beyin sapı nükleusu olan nucleus pedunculopontinus (PPN), lokomotor hareketlerin oluşumunda ve kontrolünde rol oynar. Bunun yanı sıra, PPN, uyku/uyanıklık, davranış, öğrenme ve dikkat ile de ilişkilendirilmiştir. PPN içinde kolinerjik glutamaterjik, dopaminerjik, nöradrenerjik ve GABAerjik nöronlar tanımlanmıştır. PPN son dönemlerde Parkinson hastalığının aksial semptomlarının tedavisi için potansiyel bir hedef haline gelmiştir. Protein sentezi ve salınımı sırasında gerek duyulan önemli bir molekül olan kalsiyum bağlayıcı protein ailesi üyesi kalbindin, nörodejeneratif hastalıklarla ilişkilendirilmektedir. Amacımız, bu çalışma ile GABAerjik ve glutamaterjik nöronlarla yakından ilişkili olan kalbindinin PPN’de gelişimsel olarak sentezlenme farklılıklarını incelemektir. Gereç ve Yöntem: PPN sınırları, içerdiği kolinerjik nöronlara göre tanımlanmıştır. Kalbindin, glutamaterjik ve GABAerjik nöronlardan sentezlenir. Wistar sıçanlar doğumlarının 7.gün, 14. gün ve 21. günlerinde alınarak % 4’lük paraformaldehit ile transkardiyak perfüze edilip, beyinleri çıkarılmıştır. 40 µm’luk kesitler mikrotom kullanılarak alınmış ve kesitlere immunohistokimyasal anti kolinasetil transferaz boyama ile kalbindin boyama uygulanmıştır. Çalışmamızda, her bir hayvan grubu için 4’er tane olmak üzere 12 sıçan kullanılmıştır. 7 gün, 14 gün ve 21 günlük sıçanların PPN nüklesuna ait kalbindin pozitif nöronlarının sayı, lokasyon ve nükleus çapları araştırılmıştır. Bulgular: Ortalama nöron sayıları 7 günlük hayvan için 30±3, 14 günlük hayvan için 11±1 ve 21 günlük hayvan için 150±50 olarak sayılmıştır. Nöron sayıları açısından 7. ve 14. günler ile 14 ile 21. günler arasında anlamlı farklılıklar gözlenmiştir (p=0,0075 ve p=0,0343 ).Nöron çapları 7. günde 13±1,4 µm ;14.günde 11±1,6 µm ve 21. günde 13,5±1,1 µm olarak ölçülmüştür. Sonuç: Bu çalışma, PPN’deki gelişimsel farklılıkların ortaya çıktığı kritik dönemin yukarıda belirtilen zaman aralığında olduğunu göstermiştir. Elde ettiğimiz sonuçlar, daha önce yapılan çalışmaların sonuçlarını destekleyip, katkı sağlamaktadır.

Keywords

Nucleus pedunculopontinus tegmenti Kalbindin GABAerjik Kolinerjik

References

  • 1. Garcia-Rill E. The pedunculopontine nucleus. Prog Neurobiol 1991; 36:363–89. doi:10.1016/0301-0082(91)90016-T
  • 2. Mena-Segovia J, Ross HM, Magill PJ, Bolam JP. The pedunculopontine nucleus: towards a functional integration with the basal ganglia. In: Bolam JP, Ingham JA, Magill PJ, editors. The Basal Ganglia VIII. Advances in Behavioral Biology. Volume 56. New York: Springer Science and Business Media, 2005:533-44.
  • 3. Pahapill PA, Lozano AM. The pedunculopontine nucleus and Parkinson’s disease. Brain 2000; 123:1767–83. doi: 10.1093/ brain/123.9.1767
  • 4. Pereira EA, Muthusamy KA, De Pennington N, Joint CA, Aziz TZ. Deep brain stimulation of the pedunculopontine nucleus in Parkinson’s disease. Preliminary experience at Oxford. Br J Neurosurg 2008; 22 Suppl 1:S41-4. doi:10.1080/02688690802448335.
  • 5. Mena-Segovia J, Micklem BR, Nair-Roberts RG, Ungless MA, Bolam JP. GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J Comp Neuro 2009; 515:397-408. doi: 10.1002/cne.22065.
  • 6. Semba K, Reiner PB, Fibiger HC. Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 1990; 38:643– 54. doi:10.1016/0306-4522(90)90058-C
  • 7. Semba K, Reiner PB, McGeer EG, Fibiger HC. Brainstem afferents to the magnocellular basal forebrain studied by axonal transport immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 1988; 267:433– 53.
  • 8. Lavoie B, Parent A. Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neuronsin the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 1994; 344:190–209.
  • 9. Clarke NP, Bevan MD, Cozzari C, Hartman BK, Bolam JP. Glutamate-enriched cholinergic synaptic terminals in the entopeduncular nucleus and subthalamic nucleus of the rat. Neuroscience 1997;2:371-85. doi:10.1016/S03064522(97) 00247-9
  • 10. Mena-Segovia J, Bolam JP, Magill PJ. Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family. Trends Neurosci 2004;10:585-8. doi:10.1016/ j.tins.2004.07.009
  • 11. Bolam JP, Francis CM, Henderson Z. Cholinergic input to dopaminergic neurons in the substantia nigra: a double immunocytochemical study. Neuroscience 1991;41:483-94.
  • 12. Garzon M, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM. Cholinergic axon terminals in the ventral tegmental area target a subpopulation of neurons expressing low levels of the dopamine transporter. J Comp Neurol 1999;410:197-210.
  • 13. Celio MR, Heizmann CW. Calcium-binding protein parvalbumin as a neuronal marker. Nature 1981;293:300-2.
  • 14. Baimbridge KG, Celio MR, Rogers JH. Calcium-binding proteins in the nervous system.Trends Neurosci 1992 ;15:303- 8.
  • 15. Härtig W, Brückner G, Brauer K, Seeger G, Bigl V. Triple immunofluorescence labelling of parvalbumin, calbindinD28k and calretinin in rat and monkey brain. J Neurosci Meth 1996 ;67:89-95.
  • 16. Lander ES, Linton LM, Birren B, NusbaumC, Zody MC, Baldwin J. Initial sequencing and analysis of the human genome. Nature 2001; 409:860–921.
  • 17. Celio MR. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 1990 ;35:375-475.
  • 18. Fortin M, Parent A. Calretinin-immunoreactive neurons in primate pedunculopontine and laterodorsal tegmental nuclei. Neuroscience 1999 ;88:535-47.
  • 19. Dun NJ, Dun SL, Hwang LL, Förstermann U. Infrequent co-existence of nitric oxide synthase and parvalbumin, calbindin and calretinin immunoreactivity in rat pontine neurons. Neurosci Lett 1995 26;191:165-8.
  • 20. Martinez-Gonzalez C, Micklem B R, Bolam JP, MenaSegovia J. Neurons containing calciumbinding proteins are topographically organized in the pedunculopontine nucleus. Program No. 845.17. 2009 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2009.
  • 21. Martinez-Gonzalez C, Bolam JP, Mena-Segovia J. Topographical organization of the pedunculopontine nucleus. Front Neuroanat 2011;5:22.
  • 22. Seto-Ohshima A, Emson PC, Lawson E, Mountjoy CQ, Carrasco LH. Loss of matrix calcium-binding proteincontaining neurons in Huntington’s disease. Lancet 1988; 1:1252-5.
  • 23. Côté PY, Parent A. Calbindin D-28k and choline acetyltransferase are expressed by different neuronal populations inpedunculopontine nucleus but not in nucleus basalis in squirrel monkeys Brain Res 1992 16;593:245-52.
  • 24. Tsuboi K, Kimber TA, Shults CW. Calretinin-containing axons and neurons are resistant to an intrastriatal 6-hydroxydopamine lesion. Brain Res 2000 ; 866:55-64.
  • 25. Bay KD, Mamiya K, Good CH, Skinner RD, Garcia-Rill E. Alpha-2 adrenergic regulation of pedunculopontine nucleus neurons during development. Neuroscience 2006; 141: 769–79.
  • 26. Simon C, Hayar A, Garcia-Rill E. Responses of developing pedunculopontine neurons to glutamate receptor agonists. J Neurophysiol 2011;105:1918-31. doi: 10.1152/jn.00953.2010.
  • 27. Jouvet-Mounier D, Astic L, Lacote D. Ontogenesis of thestates of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol 1970; 2: 216–39.
  • 28. Garcia-Rill E, Charlesworth A, Heister D, Ye M, Hayar A. The developmental decrease in REM sleep: the role of transmitters and electrical coupling. Sleep 2008;31:673-90.
  • 29. Thakkar M, Portas C, McCarley RW. Chronic low-amplitude electrical stimulation of the laterodorsal tegmental nucleus of freely moving cats increases REM sleep. Brain Res 1989; 723:223–27. doi:10.1016/0006-8993(96)00256-9
  • 30. Webster HH, Jones BE. Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in cat. II. Effects upon sleep-waking states. Brain Res 1988; 458:285–302. doi:10.1016/0006-8993(88)90471-4
  • 31. Steriade M, Datta S, Pare D, Oakson G, Curro Dossi R. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 1990; 10: 2541–59.
  • 32. Kobayashi T, Good C, Mamiya K, Skinner RD, Garcia-Rill E. Development of REM sleep drive and clinical implications. J Appl Physiol 2004; 96: 735–46. doi: 10.1152/japplphysiol. 00908.2003
  • 33. Kobayashi T, Good C, Biedermann J, Barnes C, Skinner RD, Garcia-Rill E. Developmental changes in pedunculopontine nucleus (PPN) neurons. J Neurophysiol 2004 ; 91:1470- 81. doi: 10.1152/jn.01024.2003
  • 34. Acsády L, Halasy K, Freund TF. Calretinin is present in nonpyramidal cells of the rat hippocampus--III. Their inputs from the median raphe and medial septal nuclei. Neuroscience 1993;52:829-41. doi:10.1016/0306-4522(93)90532-K
  • 35. Staiger JF, Masanneck C, Schleicher A, Zuschratter W. Calbindin containing interneurons are a target for VIPimmunoreactive synapses in rat primary somatosensory cortex. J Comp Neurol 2004;468:179-89. doi: 10.1002/cne.10953
  • 36. Parent M, Lévesque M, Parent A. Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J Comp Neurol 2001;439:162-75. doi: 10.1002/cne.1340
  • 37. Bhagwandin A, Gravett N, Bennett NC, Manger PR. Distribution of parvalbumin calbindin and calretinin containing neurons and terminal networks in relation to sleep associated nuclei in the brain of the giant Zambian mole-rat (Fukomys mechowii). J Chem Neuroanat 2013;52:69-79. doi: 10.1016/j.jchemneu.2013.06.002.
There are 37 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Özlem Kirazlı This is me

Ümit Şehirli This is me

Publication Date March 30, 2015
Published in Issue Year 2014 Volume: 27 Issue: 3

Cite

APA Kirazlı, Ö., & Şehirli, Ü. (2015). Nucleus pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel olarak incelenmesi. Marmara Medical Journal, 27(3), 171-177. https://doi.org/10.5472/MMJ.2014.03507.1
AMA Kirazlı Ö, Şehirli Ü. Nucleus pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel olarak incelenmesi. Marmara Med J. March 2015;27(3):171-177. doi:10.5472/MMJ.2014.03507.1
Chicago Kirazlı, Özlem, and Ümit Şehirli. “Nucleus Pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel Olarak Incelenmesi”. Marmara Medical Journal 27, no. 3 (March 2015): 171-77. https://doi.org/10.5472/MMJ.2014.03507.1.
EndNote Kirazlı Ö, Şehirli Ü (March 1, 2015) Nucleus pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel olarak incelenmesi. Marmara Medical Journal 27 3 171–177.
IEEE Ö. Kirazlı and Ü. Şehirli, “Nucleus pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel olarak incelenmesi”, Marmara Med J, vol. 27, no. 3, pp. 171–177, 2015, doi: 10.5472/MMJ.2014.03507.1.
ISNAD Kirazlı, Özlem - Şehirli, Ümit. “Nucleus Pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel Olarak Incelenmesi”. Marmara Medical Journal 27/3 (March 2015), 171-177. https://doi.org/10.5472/MMJ.2014.03507.1.
JAMA Kirazlı Ö, Şehirli Ü. Nucleus pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel olarak incelenmesi. Marmara Med J. 2015;27:171–177.
MLA Kirazlı, Özlem and Ümit Şehirli. “Nucleus Pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel Olarak Incelenmesi”. Marmara Medical Journal, vol. 27, no. 3, 2015, pp. 171-7, doi:10.5472/MMJ.2014.03507.1.
Vancouver Kirazlı Ö, Şehirli Ü. Nucleus pedunculopontinus tegmenti’de nörokimyasal özelliklerin gelişimsel olarak incelenmesi. Marmara Med J. 2015;27(3):171-7.