Spiny neurons lacking choline acetyltransferase immunoreactivity are major targets of cholinergic and catecholaminergic terminals in rat striatum
- 1 March 1990
- journal article
- research article
- Published by Wiley in Journal of Neuroscience Research
- Vol. 25 (3) , 263-280
- https://doi.org/10.1002/jnr.490250302
Abstract
The ultrastructural substrate for functional interactions between intrinsic cholinergic neurons and catecholaminergic afferents to the caudate‐putamen nucleus and nucleus accumbens septi (NAS) was investigated immunocytochemically. Single sections of glutaraldehyde‐fixed rat brain were processed (1) for the immunoperoxidase labeling of a rat monoclonal antibody against the acetylcholine‐synthesizing enzyme choline acetyltransferase (CAT) and (2) for the immunoautoradiographic localization localization of a rabbit polyclonal antiserum against the catecholamine‐synthesizing enzyme tyrosine hydroxylase (TH). The ultrastructural morphology and cellular associations did not significantly differ in the caudate‐putamen versus NAS. Immunoperoxidase reaction for CAT was seen in perikarya, dendrites, and terminals, whereas immunoautoradiography for TH was in terminals. The perikarya and dendrites immunolabeled for CAT were large, sparsely spiny, and postsynaptic mainly to unlabeled axon terminals. Only 2–3% of the CAT‐labeled terminals (n = 136) and less than 1% of the TH‐labeled terminals (n = 86) were apposed to, or formed synapses with, perikarya or dendrites immunoreactive for CAT. Most unlabeled and all labeled terminals formed symmetric synapses. In the same sample, 18% of the CAT and 16% of the TH‐labeled terminals were directly apposed to each other. Unlabeled dendritic shafts received the major (40% for CAT versus 23% for TH) synaptic input from cholinergic terminals, while unlabeled spines received the major (47% for TH versus 23% for CAT) synaptic input from catecholaminergic terminals. Neither the unlabeled dendrites or spines received detectable convergent input from CAT and TH‐labeled terminals. Thirteen percent of the CAT‐labeled and 14% of TH‐labeled terminals were in apposition to unlabeled terminals forming asymmetric, presumably excitatory, synapses with unlabeled dendritic spines. We conclude that in both the caudateputamen and NAS cholinergic and catecholaminergic terminals (1) form symmetric, most likely inhibitory, synapses primarily with non‐cholinergic neurons, (2) differentially synapse on shafts or spines of separate dendrites, and (3) have axonal appositions suggesting the possibility of presynaptic physiological interactions. These results support the hypothesis that the cholinergic‐dopaminergic balance in striatal function may be mediated through inhibition of separate sets of spiny projection neurons with opposing excitatory and inhibitory functions.Keywords
This publication has 86 references indexed in Scilit:
- Stimulation of D‐2 Dopamine Receptors Decreases the Evoked In Vitro Release of [3H] Acetylcholine from Rat Neostriatum: Role of K+ and Ca2+Journal of Neurochemistry, 1989
- Glycine modulation of NMDA-evoked release of [3H]acetylcholine and [3H]dopamine from rat striatal slicesNeuroscience Letters, 1989
- Independent gabaergic and cholinergic modulation of apomorphine-induced stereotyped rearing in the ratNeuropharmacology, 1988
- Neostriatal cholinergic neurons receive direct synaptic inputs from dopaminergic axonsBrain Research, 1987
- Localization of glutamic‐acid‐decarboxylase‐immunoreactive axon terminals in the inferior olive of the rat, with special emphasis on anatomical relations between GABAergic synapses and dendrodendritic gap junctionsJournal of Comparative Neurology, 1986
- Substance K, a novel tachykinin injected bilaterally into the ventral tegmental area of rats increases behavioral responseLife Sciences, 1985
- Organization of the efferent projections of the nucleus accumbens to pallidal, hypothalamic, and mesencephalic structures: A tracing and immunohistochemical study in the catJournal of Comparative Neurology, 1984
- Apparent lack of a dopaminergic-cholinergic link in the rat nucleus accumbens septi-tuberculum olfactoriumBrain Research, 1977
- Turnover times of gamma-aminobutyric acid and acetylcholine in nucleus caudatus, nucleus accumbens, globus pallidus and substantia nigra: effects of repeated administration of haloperidolBrain Research, 1977
- ?In vivo? release of endogenous neurotransmitters in cat limbic regions: Effect of chlorpromazine and of electrical stimulationNaunyn-Schmiedebergs Archiv für experimentelle Pathologie und Pharmakologie, 1975