Immunohistochemical study of the brainstem cholinergic system in the alpaca (Lama pacos) and colocalization with CGRP

https://doi.org/10.4081/ejh.2021.3266

Authors

  • Pilar Marcos | Pilar.Marcos@uclm.es Cellular Neuroanatomy and Molecular Chemistry of Central Nervous System, Faculty of Medicine, University of Castilla-La Mancha, CRIB (Regional Centre of Biomedical Research), Albacete, Spain. https://orcid.org/0000-0001-6303-1654
  • Rafael Coveñas Institute of Neurosciences of Castilla y León (INCYL), Laboratory of Neuroanatomy of the Peptidergic Systems; Grupo GIR USAL: BMD (Bases Moleculares del Desarrollo), University of Salamanca, Spain.

Abstract

Several cholinergic regions have been detected in the brainstem of mammals. In general, these regions are constant among different species, and the nuclear complement is maintained in animals belonging to the same order. The cholinergic system of the brainstem has been partially described in Cetartiodactyla, except for the medulla oblongata. In this work carried out in the alpaca, the description of the cholinergic regions in this order is completed by the immunohistochemical detection of the enzyme choline acetyltransferase (ChAT). In addition, using double immunostaining techniques, the relationship between the cholinergic system and the distribution of calcitonin gene-related peptide (CGRP) previously described is analysed. Although these two substances are found in several brainstem regions, the coexistence in the same cell bodies was observed only in the laterodorsal tegmental nucleus, the nucleus ambiguus and the reticular formation. These results suggest that the interaction between ChAT and CGRP may be important in the regulation of voluntary movements, the control of rapid eye movement sleep and states of wakefulness as well as in reward mechanisms. Comparing the present results with others previously obtained by our group regarding the catecholaminergic system in the alpaca brainstem, it seems that CGRP may be more functionally related to the latter system than to the cholinergic system.

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References

Davimes JG, Alagaili AN, Bennett NC, Mohammed OB, Bhagwandin A, Manger PR, et al. Neurochemical organization and morphology of the sleep related nuclei in the brain of the Arabian oryx, Oryx leucoryx. J Chem Neuroanat 2017;81:53-70. DOI: https://doi.org/10.1016/j.jchemneu.2017.02.002

Dell LA, Karlsson KA, Patzke N, Spocter MA, Siegel JM, Manger PR. Organization of the sleep-related neural systems in the brain of the minke whale (Balaenoptera acutorostrata). J Comp Neurol 2015;524:2018-35. DOI: https://doi.org/10.1002/cne.23931

Dell LA, Patzke N, Spocter MA, Bertelsen MF, Siegel JM, Manger PR. Organization of the sleep-related neural systems in the brain of the river hippopotamus (Hippopotamus amphibius): a most inusual Certiodactyl species. J Comp Neurol 2015;524:2036-58. DOI: https://doi.org/10.1002/cne.23930

Dell LA, Patzke N, Spocter MA, Siegel JM, Manger PR. Organization of the sleep-related neural systems in the brain of the harbour porpoise (Phocoena phocoena). J Comp Neurol 2016;524:1999-2017. DOI: https://doi.org/10.1002/cne.23929

Malungo IB, Gravett N, Bhagwandin A, Davimes JG, Manger PR. A preliminary description of the sleep-related neural systems in the brain of the blue wildebeest, Connochaetes taurinus. Anat Rec 2020;303:1977-97. DOI: https://doi.org/10.1002/ar.24265

De Souza E, Yi P, Aguilar LA, Coveñas R, Lerma L, Andrade R, et al. Mapping of leucine-encephalin in the alpaca (Lama pacos) brainstem. In: Coveñas R, Mangas A, Narváez JA, editors. Focus on neuropeptide research. Trivandrum: Transworld Research Network; 2007. p. 103-13.

De Souza E, Coveñas R, Yi P, Aguilar LA, Lerma L, Andrade R, et al. Mapping of CGRP in the alpaca (Lama pacos) brainstem. J Chem Neuroanat 2008;35:346-55. DOI: https://doi.org/10.1016/j.jchemneu.2008.02.004

Badlangana NL, Bhagwandin A, Fuxe K, Manger PR. Observations on the giraffe central nervous system related to the corticospinal tract, motor cortex and spinal cord: what difference does a long neck make? Neuroscience 2007;148:522-34. DOI: https://doi.org/10.1016/j.neuroscience.2007.06.005

Marcos P, Arroyo-Jiménez MM, Lozano G, Aguilar LA, Coveñas R. Mapping of tyrosine hydroxylase in the alpaca (Lama pacos) brainstem and colocalization with CGRP. J Chem Neuroanat 2011;41:63-72. DOI: https://doi.org/10.1016/j.jchemneu.2010.10.002

Coveñas R, Mangas A, Medina LE, Sánchez ML, Aguilar LA, Díaz-Cabiale Z, et al. Mapping of somatostatin-28 (1-12) in the alpaca diencephalon. J Chem Neuroanat 2011;42:89-98. DOI: https://doi.org/10.1016/j.jchemneu.2011.06.006

Marcos P, Arroyo-Jiménez MM, Lozano G, González-Fuentes J, Lagartos-Donate MJ, Aguilar LA, et al. Mapping of tyrosine hydroxylase in the diencephalon of alpaca (Lama pacos) and co-distribution with somatostatin-28 (1-12). J Chem Neuroanat 2013;50-51:66-74. DOI: https://doi.org/10.1016/j.jchemneu.2013.02.006

Manger PR. Establishing order at the systems level in mammalian brain evolution. Brain Res Bull 2005;66:282-9. DOI: https://doi.org/10.1016/j.brainresbull.2005.05.002

Badlangana NL, Bhagwandin A, Fuxe K, Manger PR. Distribution and morphology of putative catecholaminergic and serotonergic neurons in the medulla oblongata of a sub-adult giraffe, Giraffa camelopardalis. J Chem Neuroanat 2007;34:69-79. DOI: https://doi.org/10.1016/j.jchemneu.2007.05.003

Bux F, Bhagwandin A, Fuxe K, Manger PR. Organization of cholinergic, putative catecholaminergic and serotonergic nuclei in the diencephalon, midbrain and pons of sub-adult male giraffes. J Chem Neuroanat 2010;39:189-203. DOI: https://doi.org/10.1016/j.jchemneu.2009.09.006

Ferreira G, Meurisse M, Tillet Y, Lévy F. Distribution and co-localization of choline acetyltransferase and P75 neurotrophin receptors in the sheep basal forebrain: implications of the use of a specific cholinergic immunotoxin. Neuroscience 2001;104:419-39. DOI: https://doi.org/10.1016/S0306-4522(01)00075-6

Armstrong DM, Saper CB, Levey AI, Wainer BH, Terry RD. Distribution of cholinergic neurons in rat brain: demonstrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 1986;216:53-68. DOI: https://doi.org/10.1002/cne.902160106

Dell LA, Gruger JL, Bhagwandin A, Jillani NE, Pettigrew JD, Manger PR. Nuclear organization of cholinergic, putative catecholaminergic, and serotonergic systems in the brains of two megachiropteran species. J Chem Neuroanat 2010;40:177-95. DOI: https://doi.org/10.1016/j.jchemneu.2010.05.008

Cortés R, Arvidsson U, Schalling M, Ceccatelli S, Hökfelt T. In situ hybridization studies on mRNAs for cholecystokinin, calcitonin gene-related peptide and choline acetyltransferase in the lower brain stem, spinal cord and dorsal root ganglia of rat and guinea pig with special reference to motoneurons. J Chem Neuroanat 1990;3:467-85.

Henderson Z. Overlap in the distribution of cholinergic and catecholaminergic neurons in the upper brainstem of the ferret. J Comp Neurol 1987;265:581-92. DOI: https://doi.org/10.1002/cne.902650409

Henderson Z, Sherriff FE. Distribution of choline acetyltransferase immunoreactive axons and terminals in the rat and ferret brainstem. J Comp Neurol 1991;314:147-63. DOI: https://doi.org/10.1002/cne.903140114

Houser CR, Crawford GD, Barber RP, Salvaterra PM, Vaughn JE. Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res 1983;266:97-119. DOI: https://doi.org/10.1016/0006-8993(83)91312-4

Jones BE, Beaudet A. Distribution of acetylcholine and catecholamine neurons in the cat brainstem: a choline acetyltransferase and tyrosine hydroxylase immunohistochemical study. J Comp Neurol 1987;261:15-32. DOI: https://doi.org/10.1002/cne.902610103

Kimura H, Maeda T. Aminergic and cholinergic systems in the dorsolateral pontine tegmentum. Brain Res Bull 1982;9:493-9. DOI: https://doi.org/10.1016/0361-9230(82)90157-5

Levey AI, Wainer BH, Mufson EJ, Mesulam MM. Co-localization of acetylcholinesterase and choline acetyltransferase in the rat cerebrum. Neuroscience 1983;9:9-22. DOI: https://doi.org/10.1016/0306-4522(83)90042-8

Manaye KF, Zweig R, Wu D, Hersh LB, de Lacalle S, Saper CB, et al. Quantification of cholinergic and select non-cholinergic mesopontine neuronal populations in the human brain. Neuroscience 1999;89:759-70. DOI: https://doi.org/10.1016/S0306-4522(98)00380-7

Marcos P, Coveñas R, Neuroanatomical relationship between the cholinergic and tachykininergic systems in the adult human brainstem: an immunohistochemical study. J Chem Neuroanat 2019;102:101701. DOI: https://doi.org/10.1016/j.jchemneu.2019.101701

Mesulam MM. Cholinergic pathways and the ascending reticular activating system of the human brain. Ann NY Acad Sci 1995;757:169-79. DOI: https://doi.org/10.1111/j.1749-6632.1995.tb17472.x

Motts SD, Slusarczyk AS, Sowick CS, Schofield BR. Distribution of cholinergic cells in guinea pig brainstem. Neuroscience 2008;154:186-96. DOI: https://doi.org/10.1016/j.neuroscience.2007.12.017

Nakamura Y, Hassler R, Kataoka K, Bak IJ, Kim JS. Regional distribution of choline acetyltransferase and acetylcholinesterase activity in baboon brain. Folia Psychiatr Neurol Jpn 1976;30:186-94. DOI: https://doi.org/10.1111/j.1440-1819.1976.tb00121.x

Oda Y. Choline acetyltransferase: the structure, distribution and pathologic changes in the central nervous system. Pathol Int 1999;49:921-37. DOI: https://doi.org/10.1046/j.1440-1827.1999.00977.x

Oda Y, Nakanishi I. The distribution of cholinergic neurons in the human central nervous system. Histol Histopathol 2000;15:825-34.

Sakai K, Luppi PH, Salvert D, Kimura H, Maeda T, Jouvet M. Localization of cholinergic neurons in the cat lower brainstem. C R Acad Sci III 1986;303:317-24.

Satoh K, Fibiger HC. Distribution of central cholinergic neurons in the baboon (Papio papio). I. General morphology. J Comp Neurol 1985;236:197-214. DOI: https://doi.org/10.1002/cne.902360205

Satoh K, Fibiger HC. Distribution of central cholinergic neurons in the baboon (Papio papio). II. A topographic atlas correlated with catecholamine neurons. J Comp Neurol 1985;236:215-33. DOI: https://doi.org/10.1002/cne.902360206

Shiromani PJ, Armstrong DM, Berkowitz A, Jeste DV, Gillin JC. Distribution of choline acetyltransferase immunoreactive somata in the feline brainstem: implications for REM sleep generation. Sleep 1988;11:1-16. DOI: https://doi.org/10.1093/sleep/11.1.1

Tago H, McGeer PL, McGeer EG, Akiyama H, Hersh LB. Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res 1989;495:271-97. DOI: https://doi.org/10.1016/0006-8993(89)90221-7

Yasuhara O, Aimi Y, Matsuo A, Kimura H. Distribution of a splice variant of choline acetyltransferase in the trigeminal ganglion and brainstem of the rat: comparison with calcitonin gene-related peptide and substance P. J Comp Neurol 2008;509:436-48. DOI: https://doi.org/10.1002/cne.21754

Batten TF, Lo VK, Maqbool A, McWilliam PN. Distribution of calcitonin gene-related peptide-like immunoreactivity in the medulla oblongata of the cat, in relation to choline acetyltransferase-immunoreactive motoneurones and substance P-immunoreactive fibres. J Chem Neuroanat 1989;2:163-76.

Marcos P, Corio M, Dubourg P, Tramu G. Reciprocal synaptic connections between neurotensin- and tyrosine hydroxylase-immunoreactive neurons in the mediobasal hypothalamus of the guinea pig. Brain Res 1996;715:63-70. DOI: https://doi.org/10.1016/0006-8993(95)01546-9

Mesulam MM, Geula C, Bothwell MA, Hersh LB. Human reticular formation: cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons. J Comp Neurol 1989;283:611-33. DOI: https://doi.org/10.1002/cne.902830414

Ichikawa T, Ajiki K, Matsuura J, Misawa H. Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: in situ hybridization histochemistry and immunohistochemistry. J Chem Neuroanat 1997;13:23-39. DOI: https://doi.org/10.1016/S0891-0618(97)00021-5

Trifonov S, Houtani T, Hamada S, Kase M, Maruyama M, Sugimoto T. In situ hybridization study of the distribution of choline acetyltransferase mRNA and its splice variants in the mouse brain and spinal cord. Neuroscience 2009;159:344-57. DOI: https://doi.org/10.1016/j.neuroscience.2008.12.054

Lévy F, Meurisse M, Ferreira G, Thibault J, Tillet Y. Afferents to the rostral olfactory bulb in sheep with special emphasis in the cholinergic, noradrenergic and serotonergic connections. J Chem Neuroanat 1999;16:245-63. DOI: https://doi.org/10.1016/S0891-0618(99)00005-8

Mena-Segovia J. Structural and functional considerations of the cholinergic brainstem. J Neural Transm 2016;123:731-6. DOI: https://doi.org/10.1007/s00702-016-1530-9

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Published
2021-07-19
Keywords:
Alpaca, brainstem, calcitonin gene-related peptide, cholinergic system, immunohistochemistry
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How to Cite
Marcos, P., & Coveñas, R. (2021). Immunohistochemical study of the brainstem cholinergic system in the alpaca (<em>Lama pacos</em>) and colocalization with CGRP. European Journal of Histochemistry, 65(s1). https://doi.org/10.4081/ejh.2021.3266

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