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Bazal Önbeyin Kolinerjik Hücrelerinin Elektrofizyolojik Analizi

Year 2020, Volume: 2 Issue: 1, 9 - 15, 30.06.2020

Abstract

İlk mikrodiyaliz ve elektoensefalogram (EEG) çalışmalarından beri asetilkolinin bilinç üzerindeki uyarıcı etkileri bilinmektedir. Elektrofizyolojik tekniklerdeki ilerlemeler ve bu tekniklerin anatomik metodlarla harmanlanması sayesinde asetilkolinin uyanıklık süreçlerindeki rolü hakkında geçmiş bulguları destekleyici ve genişletici bilgilere ulaşılmıştır. Uyku/uyanıklık regülasyonuna ek olarak, asetilkolinin öğrenme ve bellekteki önemli rolü de yeni çalışmalarda desteklenmektedir. Kortekse asetilkolin girdisini sağlayan bazal önbeyindeki kolinerjik hücrelerin hem içsel hem de sinaptik elektrofizyolojik özelliklerini anlamak bu bağlamda çok önemlidir. Bu derleme makalesinde, bazal önbeyin kolinerjik hücreleri hakkındaki elektrofizyolojik bulgular ve literatürdeki eksiklikler tartışılmaktadır.

References

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  • Allen TGJ, Sim JA, Brown DA (1993) The whole-cell calcium current in acutely dissociated magnocellular basal forebrain neurones of the rat. J Physiol 460:91-116.
  • Alonso A, Khateb A, Fort P, Jones BE, Muhlethaler M (1996) Differential oscillatory properties of cholinergic and noncholinergic nucleus basalis neurons in guinea pig brain slice. Eur J Neurosci 8:169-182.
  • Amaral DG, Kurz J (1985) An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J Comp Neurol 240:37-59.
  • Burk, J. A., Maness, E. B., Blumenthal, S. A., & Fadel, J. R. (2019). Orexins and Cognition: Neuroanatomical and Neurochemical Substrates. In The Orexin/Hypocretin System (pp. 139-153). Academic Press.
  • Chowdhury, S., Hung, C. J., Izawa, S., Inutsuka, A., Kawamura, M., Kawashima, T., ... & Yamanaka, A. (2019). Dissociating orexin-dependent and-independent functions of orexin neurons using novel orexin-Flp knock-in mice. eLife, 8, e44927.
  • Colangelo, C., Shichkova, P., Keller, D., Markram, H., & Ramaswamy, S. (2019). Cellular, synaptic and network effects of acetylcholine in the neocortex. Frontiers in Neural Circuits, 13.
  • Cullinan WE, Zaborszky L (1991) Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons. J Comp Neurol 306:631-667.
  • Damborsky, J. C., Smith, K. G., Jensen, P., & Yakel, J. L. (2017). Local cholinergic-GABAergic circuitry within the basal forebrain is modulated by galanin. Brain Structure and Function, 222(3), 1385-1400.
  • Descarries L, Mechawar N, Aznavour N, Watkins KC (2004) Structural determinants of the roles of acetylcholine in cerebral cortex. Progr Brain Res 145:45-59.
  • Duque A, Balatoni B, Detari L, Zaborszky L (2000) EEG correlation of the discharge properties of identified neurons in the basal forebrain. J Neurophysiol 84:1627-1685.
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  • Katz B, Miledi R (1966) The release of acetylcholine from nerve endings by graded electrical pulses. Proc Roy Soc 167:23-38.
  • Khateb A, Fort P, Pegna A, Jones BE, Mühlethaler M (1995) Cholinergic nucleus basalis neurons are excited by histamine in vitro. Neuroscience 69:495-506.
  • Khateb A, Fort P, Williams S, Serafin M, Jones BE, Mühlethaler M (1997) Modulation of cholinergic nucleus basalis neurons by acetylcholine and N-methyl-D-aspartate. Neuroscience 81:47-55.
  • Krnjevic K, Phillis, JW (1963) Actions of certain amines on cerebral cortical neurones. Br J Pharmacol Chemother 20:471-490.
  • Kroeger, D., Absi, G., Gagliardi, C., Bandaru, S. S., Madara, J. C., Ferrari, L. L., ... & Vetrivelan, R. (2018). Galanin neurons in the ventrolateral preoptic area promote sleep and heat loss in mice. Nature communications, 9(1), 4129.
  • Lee, M. G., Hassani, O. K., Alonso, A., & Jones, B. E. (2005). Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. Journal of Neuroscience, 25(17), 4365-4369.
  • Leranth C, Vertes RP (1999) Median raphe serotonergic innervation of medial septum/diagonal band of broca (MSDB) parvalbumin-containing neurons: possible involvement of the MSDB in the desynchronization of the hippocampal EEG. J Comp Neurol 410:586-598.
  • Li, X., Yu, B., Sun, Q., Zhang, Y., Ren, M., Zhang, X., ... & Zeng, H. (2018). Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons. Proceedings of the National Academy of Sciences, 115(2), 415-420.
  • López-Hernández, G. Y., Ananth, M., Jiang, L., Ballinger, E. C., Talmage, D. A., & Role, L. W. (2017). Electrophysiological properties of basal forebrain cholinergic neurons identified by genetic and optogenetic tagging. Journal of neurochemistry, 142, 103-110.
  • Luskin MB, Price JL (1982) The distribution of axon collaterals from the olfactory bulb and the nucleus of the horizontal limb of the diagonal band to the olfactory cortex, demonstrated by double retrograde labeling technique. J Comp Neurol 209:249-263.
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  • Markram H, Segal M (1990) Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res 513:171-174.
  • McDonald AJ (1991) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44:1-14.
  • McKenna, J. T., Yang, C., Franciosi, S., Winston, S., Abarr, K. K., Rigby, M. S., ... & Brown, R. E. (2013). Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse. Journal of Comparative Neurology, 521(6), 1225-1250.
  • Meller, S., Brandt, C., Theilmann, W., Klein, J., & Löscher, W. (2019). Commonalities and differences in extracellular levels of hippocampal acetylcholine and amino acid neurotransmitters during status epilepticus and subsequent epileptogenesis in two rat models of temporal lobe epilepsy. Brain research, 1712, 109-123.
  • Mesulam MM, Mufson EJ (1984) Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 107:253-274.
  • Momiyama T, Zaborszky L (2006) Somatostatin presynaptically inhibits both GABA and glutamate release onto rat basal forebrain cholinergic neurons. J Neurophysiol 96:686-694.
  • Mrzljak L, Pappy M, Leranth C, Goldman-Rakic PS (1995) Cholinergic synaptic circuitry in the macaque prefrontal cortex. J Comp Neurol 357:603-661.
  • Petrovich GD, Risold PY, Swanson LW (1996) Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 374:387-420.
  • Rubin RP (2007) A brief history of great discoveries in pharmacology: in celebration of the centennial anniversary of the founding of the American Society of Pharmacology and Experimental Therapeutics. Pharmacol Rev 59:289-359.
  • Sarter, M., Lustig, C., Howe, W. M., Gritton, H., & Berry, A. S. (2014). Deterministic functions of cortical acetylcholine. European Journal of Neuroscience, 39(11), 1912-1920.
  • Semba K (2004) Phylogenetic and ontogenetic aspects of the basal forebrain cholinergic neurons and their innervations of the cerebral cortex. Prog Brain Res 145, 3-36.
  • Simon, A. P., Poindessous-Jazat, F., Dutar, P., Epelbaum, J., & Bassant, M. H. (2006). Firing properties of anatomically identified neurons in the medial septum of anesthetized and unanesthetized restrained rats. Journal of Neuroscience, 26(35), 9038-9046.
  • Smiley JF, Morrell F, Mesulam MM (1997) Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections. Exp Neurol 144:361-368.
  • Sotty F, Danik M, Manseau F, Laplanta F, Quirion R, Williams S (2003) Distinct electrophysiological properties of glutamatergic cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J Physiol 551:927-943.
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A Summary of Electrophysiological Research of Basal Forebrain Cholinergic Neurons

Year 2020, Volume: 2 Issue: 1, 9 - 15, 30.06.2020

Abstract

Acetylcholine has been known to be a wake-promoting neurotransmitter since the earliest microdialysis studies coupled to electroencephalographic (EEG) measurements. Advances in electrophysiological recording tools tied to anatomical identification methods helped to unequivocally indicate that these neurons exhibit augmented activity during wake periods. Later studies have revealed that acetylcholine plays essential roles in higher cognitive functions such as learning and memory. Understanding the intrinsic and synaptic electrophysiology of basal forebrain cholinergic (BFc) neurons is of paramount importance for answering how the BFc neuron system fulfills all those functions. This review discusses the latter questions along with a summary of missing links in the current state of knowledge.

References

  • Adams, C., DeFazio, R. A., Christian, C. A., Milescu, L. S., Schnell, S., & Moenter, S. M. (2019). Changes in Both Neuron Intrinsic Properties and Neurotransmission Are Needed to Drive the Increase in GnRH Neuron Firing Rate during Estradiol-Positive Feedback. Journal of Neuroscience, 39(11), 2091-2101.
  • Allen TGJ, Sim JA, Brown DA (1993) The whole-cell calcium current in acutely dissociated magnocellular basal forebrain neurones of the rat. J Physiol 460:91-116.
  • Alonso A, Khateb A, Fort P, Jones BE, Muhlethaler M (1996) Differential oscillatory properties of cholinergic and noncholinergic nucleus basalis neurons in guinea pig brain slice. Eur J Neurosci 8:169-182.
  • Amaral DG, Kurz J (1985) An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J Comp Neurol 240:37-59.
  • Burk, J. A., Maness, E. B., Blumenthal, S. A., & Fadel, J. R. (2019). Orexins and Cognition: Neuroanatomical and Neurochemical Substrates. In The Orexin/Hypocretin System (pp. 139-153). Academic Press.
  • Chowdhury, S., Hung, C. J., Izawa, S., Inutsuka, A., Kawamura, M., Kawashima, T., ... & Yamanaka, A. (2019). Dissociating orexin-dependent and-independent functions of orexin neurons using novel orexin-Flp knock-in mice. eLife, 8, e44927.
  • Colangelo, C., Shichkova, P., Keller, D., Markram, H., & Ramaswamy, S. (2019). Cellular, synaptic and network effects of acetylcholine in the neocortex. Frontiers in Neural Circuits, 13.
  • Cullinan WE, Zaborszky L (1991) Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons. J Comp Neurol 306:631-667.
  • Damborsky, J. C., Smith, K. G., Jensen, P., & Yakel, J. L. (2017). Local cholinergic-GABAergic circuitry within the basal forebrain is modulated by galanin. Brain Structure and Function, 222(3), 1385-1400.
  • Descarries L, Mechawar N, Aznavour N, Watkins KC (2004) Structural determinants of the roles of acetylcholine in cerebral cortex. Progr Brain Res 145:45-59.
  • Duque A, Balatoni B, Detari L, Zaborszky L (2000) EEG correlation of the discharge properties of identified neurons in the basal forebrain. J Neurophysiol 84:1627-1685.
  • Duque A, Tepper JM, Detari L, Ascoli GA, Zaborszky L (2007) Morphological characterization of electrophysiologically and immunohistochemically identified basal forebrain cholinergic and neuropeptide Y-containing neurons. Brain Struct Funct 212:55-73.
  • Eccles JC, Fatt P, Koketsu K (1954) Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol 126:524-562.
  • Eggermann E, Serafin M, Bayer L, Machard D, Saint-Mleux B, Jones BE (2001) Orexins/hypocretins excite basal forebrain cholinergic neurons. Neuroscience 108:177-181.
  • Garrido-Sanabria ER, Perez-Cordova MG, Colom LV (2011) Differential expression of voltage-gated K+ currents in medial septum/diagonal band complex neurons exhibiting distinct firing phenotypes. Neurosci Res 70:361-369.
  • Gasbarri A, Sulli A, Pacitti C, McGaugh JL (1999) Serotonergic input to cholinergic neurons in the substantia innominata and nucleus basalis magnocellularis in the rat. Neuroscience 91:1129-1142.
  • Gielow, M. R., & Zaborszky, L. (2017). The input-output relationship of the cholinergic basal forebrain. Cell reports, 18(7), 1817-1830.
  • Griffith WH, Matthews RT (1986) Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci Lett 71:169-174.
  • Griffith WH, Sim JA, Matthews RT (1991) Electrophysiologic characteristics of basal forebrain neurons In Vitro. The Basal Forebrain Anatomy to Function. Edited by Napier TC, Kalivas PW, Hanin I. pp. 143-157. Plenum Press New York and London.
  • Grove EA (1988) Neural associations of the substantia innominata in the rat: afferent connections. J Comp Neurol 277:315-346.
  • Hajszan T, Zaborszky L (2000). Serotoninergic innervation of basal forebrain neurons in the rat. Serotonin: From the molecule to the clinic. A Serotonin Club/Brain Research Bulletin Conference, Elsevier Science, Abstract, p. 97.
  • Hajszan T, Zaborszky L (2002) Direct catecholaminergic-cholinergic interactions in the basal forebrain. III. Adrenergic innervation of choline acetyltransferase-containing neurons in the rat. J Comp Neurol 449:141-157.
  • Han SH, McCool BA, Murchison D, Nahm SS, Parrish AR, Griffith WH (2002) Single-cell RT-PCR detects shifts in mRNA expression profiles of basal forebrain neurons during aging. Brain Res Mol Brain Res 98:67-80.
  • Hangya, B., Ranade, S. P., Lorenc, M., & Kepecs, A. (2015). Central cholinergic neurons are rapidly recruited by reinforcement feedback. Cell, 162(5), 1155-1168.
  • Harrison, T. C., Pinto, L., Brock, J. R., & Dan, Y. (2016). Calcium imaging of basal forebrain activity during innate and learned behaviors. Frontiers in neural circuits, 10, 36.
  • Hasselmo, M. E., & Stern, C. E. (2018). A network model of behavioural performance in a rule learning task. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1744), 20170275.
  • Heimer L, Alheid GF (1991) Piecing together the puzzle of basal forebrain anatomy. The Basal Forebrain Anatomy to Function. Edited by Napier TC, Kalivas PW, Hanin I. pp. 253-267. Plenum Press New York and London.
  • Henderson Z, Morris NP, Grimwood P, Fiddler G, Yang HW, Appenteng K (2001) Morphology of local axon collaterals of electrophysiologically characterised neurons in the rat medial septal/ diagonal band complex. Comp Neurol 430:410-432.
  • Henny P, Jones BE (2006) Innervation of orexin/hypocretin neurons by GABAergic, glutamatergic, or cholinergic basal forebrain terminals evidenced by immunostaining for presynaptic vesicular transporter and postsynaptic scaffolding proteins. J Comp Neurol 499:645-661.
  • Iavarone, E., Yi, J., Shi, Y., Zandt, B. J., O’Reilly, C., Van Geit, W., ... & Hill, S. L. (2019). Experimentally-constrained biophysical models of tonic and burst firing modes in thalamocortical neurons. PLoS computational biology, 15(5), e1006753.
  • Kanai T, Szerb JC (1965) Mesencephalic reticular activating system and cortical acetylcholine output. Nature 205:80-82.
  • Katz B, Miledi R (1966) The release of acetylcholine from nerve endings by graded electrical pulses. Proc Roy Soc 167:23-38.
  • Khateb A, Fort P, Pegna A, Jones BE, Mühlethaler M (1995) Cholinergic nucleus basalis neurons are excited by histamine in vitro. Neuroscience 69:495-506.
  • Khateb A, Fort P, Williams S, Serafin M, Jones BE, Mühlethaler M (1997) Modulation of cholinergic nucleus basalis neurons by acetylcholine and N-methyl-D-aspartate. Neuroscience 81:47-55.
  • Krnjevic K, Phillis, JW (1963) Actions of certain amines on cerebral cortical neurones. Br J Pharmacol Chemother 20:471-490.
  • Kroeger, D., Absi, G., Gagliardi, C., Bandaru, S. S., Madara, J. C., Ferrari, L. L., ... & Vetrivelan, R. (2018). Galanin neurons in the ventrolateral preoptic area promote sleep and heat loss in mice. Nature communications, 9(1), 4129.
  • Lee, M. G., Hassani, O. K., Alonso, A., & Jones, B. E. (2005). Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. Journal of Neuroscience, 25(17), 4365-4369.
  • Leranth C, Vertes RP (1999) Median raphe serotonergic innervation of medial septum/diagonal band of broca (MSDB) parvalbumin-containing neurons: possible involvement of the MSDB in the desynchronization of the hippocampal EEG. J Comp Neurol 410:586-598.
  • Li, X., Yu, B., Sun, Q., Zhang, Y., Ren, M., Zhang, X., ... & Zeng, H. (2018). Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons. Proceedings of the National Academy of Sciences, 115(2), 415-420.
  • López-Hernández, G. Y., Ananth, M., Jiang, L., Ballinger, E. C., Talmage, D. A., & Role, L. W. (2017). Electrophysiological properties of basal forebrain cholinergic neurons identified by genetic and optogenetic tagging. Journal of neurochemistry, 142, 103-110.
  • Luskin MB, Price JL (1982) The distribution of axon collaterals from the olfactory bulb and the nucleus of the horizontal limb of the diagonal band to the olfactory cortex, demonstrated by double retrograde labeling technique. J Comp Neurol 209:249-263.
  • Manns ID, Alonso A, Jones BE (2000) Discharge properties of juxtacellularly labeled and immunohistochemically identified cholinergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J Neurosci 20:1505-1518.
  • Markram H, Segal M (1990) Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res 513:171-174.
  • McDonald AJ (1991) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44:1-14.
  • McKenna, J. T., Yang, C., Franciosi, S., Winston, S., Abarr, K. K., Rigby, M. S., ... & Brown, R. E. (2013). Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse. Journal of Comparative Neurology, 521(6), 1225-1250.
  • Meller, S., Brandt, C., Theilmann, W., Klein, J., & Löscher, W. (2019). Commonalities and differences in extracellular levels of hippocampal acetylcholine and amino acid neurotransmitters during status epilepticus and subsequent epileptogenesis in two rat models of temporal lobe epilepsy. Brain research, 1712, 109-123.
  • Mesulam MM, Mufson EJ (1984) Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 107:253-274.
  • Momiyama T, Zaborszky L (2006) Somatostatin presynaptically inhibits both GABA and glutamate release onto rat basal forebrain cholinergic neurons. J Neurophysiol 96:686-694.
  • Mrzljak L, Pappy M, Leranth C, Goldman-Rakic PS (1995) Cholinergic synaptic circuitry in the macaque prefrontal cortex. J Comp Neurol 357:603-661.
  • Petrovich GD, Risold PY, Swanson LW (1996) Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 374:387-420.
  • Rubin RP (2007) A brief history of great discoveries in pharmacology: in celebration of the centennial anniversary of the founding of the American Society of Pharmacology and Experimental Therapeutics. Pharmacol Rev 59:289-359.
  • Sarter, M., Lustig, C., Howe, W. M., Gritton, H., & Berry, A. S. (2014). Deterministic functions of cortical acetylcholine. European Journal of Neuroscience, 39(11), 1912-1920.
  • Semba K (2004) Phylogenetic and ontogenetic aspects of the basal forebrain cholinergic neurons and their innervations of the cerebral cortex. Prog Brain Res 145, 3-36.
  • Simon, A. P., Poindessous-Jazat, F., Dutar, P., Epelbaum, J., & Bassant, M. H. (2006). Firing properties of anatomically identified neurons in the medial septum of anesthetized and unanesthetized restrained rats. Journal of Neuroscience, 26(35), 9038-9046.
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Details

Primary Language English
Journal Section Review Articles
Authors

Çağrı Temuçin Ünal 0000-0003-2942-546X

Publication Date June 30, 2020
Published in Issue Year 2020 Volume: 2 Issue: 1

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APA Ünal, Ç. T. (2020). A Summary of Electrophysiological Research of Basal Forebrain Cholinergic Neurons. İzmir Sosyal Bilimler Dergisi, 2(1), 9-15.
İzmir Journal of Social Sciences © 2019
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