Cholinergic neuropil of the striatum observes striosomal boundaries

Abstract

Acetylcholine and dopamine are key neurotransmitters in the extrapyramidal motor system, where they are thought to lie in a 'functional balance' brought about by interactions between the terminals of the dopamine-containing nigrostriatal tract and the cholinergic interneurones of the striatum. The precise nature of these interactions is not understood, however, nor is it clear how they influence the functioning of striatal systems containing other neurotransmitters. A new clue to understanding such interplay among transmitter-coded systems in the striatum has come from the finding that many of them, including nigrostriatal afferents, follow a macroscopic ordering in which neural elements are concentrated either in or out of the striatal tissue compartments called striosomes. We here report that the cholinergic neuropil of the striatum is also compartmentalized: fibres expressing immunoreactivity to antibodies raised against choline acetyltransferase (ChAT) are sparse in striosomes and are dense in the extrastriosomal matrix. These findings suggest that the interactions between acetylcholine and other neurotransmitters in the striatum are spatially constrained, that cholinergic modulation of striatal function predomintes in the extrastriosomal matrix, and that extrapyramidal pathways originating in the matrix, including transthalamic pathways to the frontal lobes, may in particular reflect this cholinergic influence. Such a differential organization of striatal cholinergic circuitry could help to account for the selective therapeutic efficacy of anticholinergic drugs in the treatment of extrapyramidal disorders.

Striosome–dendron bouquets highlight a unique striatonigral circuit targeting dopamine-containing neurons

“…Much evidence suggests that cholinergic interneurons in the striatum can exert powerful control over the intrastriatal release of dopamine (34,35). We have noted that these cholinergic interneurons, although having predominant distributions at the striosome-matrix compartment borders (36), send many fine fibers into the striosomes (37,38). By contrast, cholinergic inputs from the brainstem pedunculopontine nucleus (PPN) preferentially innervate the matrix (39).…”

α6-Containing Nicotinic Acetylcholine Receptors Dominate the Nicotine Control of Dopamine Neurotransmission in Nucleus Accumbens

“…Markers of striatal cholinergic innervation (choline acetyltransferase and AChE) show dense and patchy distributions within both dorsal and ventral striatum (Graybiel et al, 1986;Holt et al, 1997;Phelps and Vaughn, 1986;Zahm and Brog, 1992) but there is not a consensus from microdialysis reports for the comparative ACh tone (eg Ichikawa et al, 2002;Parada et al, 1997). However, ambenonium in striatum has been reported to increase single-pulse-evoked DA release at low concentrations (B10 À9 -10 À8 M) but suppress DA release at higher concentrations (410 À8 M) when ACh reaches concentrations sufficient to desensitize nAChRs .…”

Tonically Active Neurons in the Primate Caudate Nucleus and Putamen Differentially Encode Instructed Motivational Outcomes of Action

“…As presumed cholinergic interneurons located mostly around the border between the striosomes and matrix in the striatum (Graybiel et al, 1986;Aosaki et al, 1995), TANs, although small in number, may play an essential role in modifying the activity of surrounding projection neurons directly (Calabresi et al, 2000; Figure 11. The response to GO was not time-locked to the onset of movement but to onset of GO.…”