Abstract
This study reports the reactivities of acetylcholinesterase (AChE) and choline acetyltransferase (ChAT) in some of the nonneuronal elements in the external cuneate nucleus (ECN) of gerbils. AChE reaction products were localized in some oligodendrocytes in their cisternae of rough endoplasmic reticulum, nuclear envelope and Golgi saccules. The basal lamina lining the capillary endothelia also displayed AChE reactivity. In ChAT immunocytochemistry, the reaction products were found to be associated with the vascular basal lamina as well as the endothelial plasma membrane facing the lumen. The most remarkable finding was the localization of ChAT immunoreactivity in some oligodendrocytes and occasional glioblasts (small glial precursor cells containing a thin rim of cytoplasm surrounding an irregular nucleus with homogeneous chromatin materials). The ChAT-positive oligodendrocytes consisted of two types, medium-dense and dark cells, either associated with blood vessels or ChAT-stained neuronal elements. It is suggested from these new findings that at least some of the oligodendrocytes and glioblasts in the ECN of gerbils may be involved in the synthesis, storage, release and degradation of acetylcholine.
Similar content being viewed by others
References
Armstrong DM (1986) Ultrastructural characterization of choline acetyltransferase-containing neurons in the basal forebrain of rat: evidence for a cholinergic innervation of intracerebral blood vessels. J Comp Neurol 250:81–92
Arnerić SP, Honig MA, Milner TA, Greco S, Iadecola C, Reis DJ (1988) Neuronal and endothelial sites of acetylcholine synthesis and release associated with microvessels in rat cerebral cortex: ultrastructural and neurochemical studies. Brain Res 454:11–30
Butt AM, Tutton M (1992) Response of oligodendrocytes to glutamate and γ-aminobutyric acid in the intact mouse optic nerve. Neurosci Lett 146:108–110
Duckles SP (1981) Evidence for a functional cholinergic innervation for cerebral arteries. J Pharmacol Exp Ther 217:544–548
Engel AK, Kreutzberg GW (1988) Neuronal surface changes in the dorsal vagal motornucleus of the guinea pig in response to axotomy. J Comp Neurol 275:181–200
Estrada C, Hamel E, Krause DN (1983) Biochemical evidence for cholinergic innervation of intracerebral blood vessels. Brain Res 266:261–270
Furchgott RF, Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373–376
Goldstein GW, Wolinsky JS, Csejtey J, Diamond J (1975) Isolation of metabolically active capillaries from rat brain. J Neurochem 25:715–717
Hamel E, Assumel-Lurdin C, Edvinsson L, Mackenzie ET (1986) Cholinergic innervation of small pial vessels: specific uptake and release processes. Acta Physiol Scand 552:13–16
Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1985) Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J Comp Neurol 234:17–34
Kaplan MS, Hinds JW (1980) Gliogenesis of astrocytes and oligodendrocytes in the neocortical grey and white matter of the adult rat: electron microscopic analysis of light radioautographs. J Comp Neurol 193:711–727
Kimelberg HK (1986a) Catecholamine and serotonin uptake in astrocytes. In: Federoff S, Vernadakis A (eds) Astrocytes: biochemistry, physiology, and pharmacology of astrocytes, vol 2. Academic Press, Orlando, Florida, pp 107–127
Kimelberg HK (1986b) Occurrence and functional significance of serotonin and catecholamine uptake by astrocytes. Biochem Pharmacol 35:2273–2281
Kimelberg HK, Goderie SK, Conley PA, Higman S, Goldschmidt R, Amundson RH (1992a) Uptake of [3H]serotonin and [3H]glutamate by primary astrocyte cultures. I. Effects of different sera and time in culture. Glia 6:1–8
Kimelberg HK, Goderie SK, Conley PA, Higman S, Goldschmidt R, Amundson RH (1992b) Uptake of [3H]serotonin and [3H]glutamate by primary astrocyte cultures. II. Differences in cultures prepared from different brain regions. Glia 6:9–18
Lan CT, Wen CY, Shieh JY (1994a) Musculotopic organization of muscle afferents in the external cuneate nucleus of the gerbil as revealed by transganglionic transport of HRP. Acta Anat 149:134–140
Lan CT, Wen CY, Shieh JY (1994b) Anatomical studies on the cuneocerebellar neurons in the gerbil by using HRP method. Ann Anat 176:409–418
Lan CT, Wen CY, Shieh JY (1994c) Cells of origin, thalamic relay and termination of the external cuneothalamocortical tract in the gerbil. Ann Anat 176:527–538
Lan CT, Wen CY, Tseng GF, Tan CK, Ling EA, Shieh JY (1994d) Efferent connections from the external cuneate nucleus to the medulla oblongata in the gerbil. Brain Res 668:107–116
Lan CT, Wen CY, Tan CK, Ling EA, Shieh JY (1995a) An ultrastructural study of cuneocerebellar neurons and primary afferent terminals in the external cuneate nucleus of gerbils as revealed by retrograde and transganglionic transport of horseradish peroxidase. J Neurocytol 24:465–477
Lan CT, Wen CY, Tan CK, Ling EA, Shieh JY (1995b) A comparative ultrastructural study of primary afferents from the brachial and cervical plexuses to the external cuneate nucleus of gerbils. J Anat 187:115–125
Lan CT, Wen CY, Tan CK, Ling EA, Shieh JY (1995c) Ultrastructural identification of cholinergic neurons in the external cuneate nucleus of the gerbil: acetylcholinesterase histochemistry and choline acetyltransferase immunocytochemistry. J Neurocytol 24:838–852
Lan CT, Wen CY, Tan CK, Ling EA, Shieh JY (1995d) Multiple origins of cerebellar cholinergic afferents from the lower brainstem in the gerbil. J Anat 186:549–561
Lan CT, Wen CY, Tan CK, Ling EA, Shieh JY (1996) Ultrastructural study of external cuneothalamic neurons and their synaptic relationships with primary afferents in the gerbil. J Comp Neurol 366:406–415
Levey AI, Armstrong DM, Atweh SF, Terry RD, Wainer BH (1983) Monoclonal antibodies to choline acetyltransferase: production, specificity, and immunohistochemistry. J Neurosci 3:1–9
Lewis PR, Knight DP (1977) Metal precipitation methods for hydrolytic enzymes. In: Glauert AM (ed) Practical methods in electron microscopy, vol 5. NHPC Press, Amsterdam, pp 137–223
Lewis PR, Shute CCD (1969) An electron-microscopic study of cholinesterase distribution in the rat adrenal medulla. J Microsc 89:181–193
Liesi P, Paetau A, Rechardt L, Dahl D (1981) Glial uptake of monoamines in primary cultures of rat median raphe nucleus and cerebellum: a combined monoamine fluorescence and glial fibrillary acidic protein immunofluorescence study. Histochemistry 73:239–250
Ling EA, Paterson JA, Privat A, Mori S, Leblond CP (1973) Investigation of glial cells in semithin sections. I. Identification of glial cells in the brain of young rats. J Comp Neurol 149:43–72
Massarelli R, Mykita S, Sorrentino G (1986) The supply of choline to glial cells. In: Fedoroff S, Vernadakis A (eds) Astrocytes: biochemistry, physiology and pharmacology of astrocytes, vol 2. Academic Press, Orlando, Florida, pp 155–178
Monzon-Mayor M, Yanes C, James JL, Sturrock RR (1990a) An ultrastructural study of the development of astrocytes in the midbrain of the lizard. J Anat 170:33–41
Monzon-Mayor M, Yanes C, James JL, Sturrock RR (1990b) An ultrastructural study of the development of oligodendrocytes in the midbrain of the lizard. J Anat 170:43–49
Mori S, Leblond CP (1970) Electron microscopic identification of three classes of oligodendrocytes and a preliminary study of their proliferative activity in the corpus callosum of young rats. J Comp Neurol 139:1–30
Parnavelas JG, Kelly W, Burnstock G (1985) Ultrastructural localization of choline acetyltransferase in vascular endothelial cells in rat brain. Nature 316:724–725
Parnavelas JG, Kelly W, Franke E, Eckenstein F (1986) Cholinergic neurons and fibres in the rat visual cortex. J Neurocytol 15:329–336
Paterson JA, Privat A, Ling EA, Leblond CP (1973) Investigation of glial cells in semithin sections III. Transformation of subependymal cells into glial cells, as shown by radioautography after 3H-thymidine injection into the lateral ventricle of the brain of young rats. J Comp Neurol 149:83–102
Reynolds R, Herschkowitz N (1986) Selective uptake of neuroactive amino acids by both oligodendrocytes and astrocytes in primary dissociated culture: a possible role for oligodendrocytes in neurotransmitter metabolism. Brain Res 371:253–266
Spencer RF, Baker R (1986) Histochemical localization of acetylcholinesterase in relation to motor neurons and internuclear neurons of the cat abducens nucleus. J Neurocytol 15:137–154
Tucek S (1985) Regulation of acetylcholine synthesis in the brain. J Neurochem 44:11–24
Vaughn JE, Barber RP, Ribak CE, Houser CR (1981) Methods for the immunocytochemical localization of proteins and peptides involved in neurotransmission. In: Johnson JE Jr (ed) Current trends in morphological techniques, vol 3. CRC Press, Boca Raton, Fla, pp 33–70
Vernadakis A (1988) Neuron-glia interrelations. Int Rev Neurobiol 30:149–224
Wainer BH, Levey AI, Mufson EJ, Mesulam MM (1984) Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase. Neurochem Int 6:163–182
Yamamura HI, Snyder SH (1972) Choline: high-affinity uptake by rat brain synaptosomes. Science 178:626–628
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lan, CT., Shieh, JY., Wen, CY. et al. Ultrastructural localization of acetylcholinesterase and choline acetyltransferase in oligodendrocytes, glioblasts and vascular endothelial cells in the external cuneate nucleus of the gerbil. Anat Embryol 194, 177–185 (1996). https://doi.org/10.1007/BF00195011
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00195011