A dopaminergic axon lattice in the striatum and its relationship with cortical and thalamic terminals - PubMed (original) (raw)
Comparative Study
A dopaminergic axon lattice in the striatum and its relationship with cortical and thalamic terminals
Jonathan Moss et al. J Neurosci. 2008.
Abstract
Interactions between glutamatergic corticostriatal afferents and dopaminergic nigrostriatal afferents are central to basal ganglia function. The thalamostriatal projection provides a glutamatergic innervation of similar magnitude to the corticostriatal projection. We tested the hypotheses that (1) thalamostriatal synapses have similar spatial relationships with dopaminergic axons as corticostriatal synapses do and (2) the spatial relationships between excitatory synapses and dopaminergic axons are selective associations. We examined at the electron microscopic level rat striatum immunolabeled to reveal vesicular glutamate transporters (VGluTs) 1 and 2, markers of corticostriatal and thalamostriatal terminals, respectively, together with tyrosine hydroxylase (TH) to reveal dopaminergic axons. Over 80% of VGluT-positive synapses were within 1 microm of a TH-positive axon and >40% were within 1 microm of a TH-positive synapse. Of structures postsynaptic to VGluT1- or VGluT2-positive terminals, 21 and 27%, respectively, were apposed by a TH-positive axon and about half of these made synaptic contact. When structures postsynaptic to VGluT-positive terminals and VGluT-positive terminals themselves were normalized for length of plasma membrane, the probability of them being apposed by, or in synaptic contact with, a TH-positive axon was similar to that of randomly selected structures. Extrapolation of the experimental data to more closely reflect the distribution in 3D reveals that all structures in the striatum are within approximately 1 microm of a TH-positive synapse. We conclude that (1) thalamostriatal synapses are in a position to be influenced by released dopamine to a similar degree as corticostriatal synapses are and (2) these associations arise from a nonselective dopaminergic axon lattice.
Figures
Figure 1.
VGluT1- and VGluT2-positive terminals contact dendritic spines and shafts in the striatum. A, VGluT1-positive bouton (b) makes asymmetrical synaptic contact (arrowhead) with the head of dendritic spine (s) which arises from a dendritic shaft (d). A TH-positive axon (TH) is present in the field and is apposed to the spine in adjoining serial sections. B, VGluT1-positive boutons (b1 and b3) make asymmetrical synapses (arrowheads) with a dendritic shaft (d). Another VGluT1-positive bouton (b2) makes asymmetrical synaptic contact (arrowhead) with a spine (s) and in adjoining serial sections (b2 inset) also makes asymmetrical synaptic contact (arrow) with the dendritic shaft (d). Note that although there are only few immunogold particles overlying boutons b2 and b3 in this section, in the remaining five serial sections additional immunogold labeling can be seen (b2 and b3 insets) confirming that they were VGluT1-positive. C, VGluT2-positive boutons b1 and b2 make asymmetrical synaptic contact (arrowheads) with a spine (s) and a dendritic shaft (d), respectively. D, A VGluT2-positive bouton (b) makes asymmetrical synaptic contact (arrowhead) with a dendritic shaft (d). A TH-positive axon (TH) is in the vicinity. Scale bars, 200 nm.
Figure 2.
Individual VGluT1- and VGluT2-positive terminals often make multiple synaptic contacts. A, A VGluT1-positive bouton (b1) makes asymmetrical synaptic contacts (arrowheads) with a spine (s) and a dendritic shaft (d). The dendritic shaft (d) is also in asymmetrical synaptic contact with an unlabeled bouton (b2). B, A VGluT1-positive bouton (b) makes asymmetrical synaptic contact (arrowheads) with three spines (s1, s2 and s3; some contacts are seen more clearly in other serial sections of the six collected). Note that although there are only few immunogold particles overlying this bouton in this section, in the remaining five serial sections additional immunogold labeling was observed (inset) confirming that it was VGluT1-positive. Also note that this bouton is apposed by a TH-positive axon (TH). C, A VGluT2-positive bouton (b) makes asymmetrical synaptic contacts (arrowheads) with two spines (s1 and s2). D, A VGluT2-positive bouton (b1) makes asymmetrical synaptic contacts (arrowheads) with two dendritic shafts (d1 and d2). Two spines (s1 and s2) are seen arising from the dendrite, d1, and both are in close proximity to TH-positive axons (TH1 and TH2, respectively). One of these spines (s1) is in asymmetrical synaptic contact (arrowhead) with an unlabeled bouton (b2). Scale bars, 200 nm.
Figure 3.
Striatal spines and dendritic shafts postsynaptic to VGlut1- or VGluT2-positive terminals are apposed by, or in synaptic contact with, TH-positive terminals. A, A VGluT1-positive bouton (b) makes asymmetrical synaptic contact (arrowhead) with the head of long thin spine (s). A TH-positive terminal (TH) makes symmetrical synaptic contact (arrow) with the neck of the same spine. B, A VGluT1-positive bouton (b1) makes asymmetrical synaptic contact with a dendritic shaft (d) which is apposed (arrow) by a TH-positive axon (TH). Within the vicinity, another VGluT1-positive bouton (b2) makes asymmetrical synaptic contact (arrowheads) with a spine (s). C, A VGluT2-positive bouton (b1) makes asymmetrical synaptic contact (arrowhead) with a spine (s) that arises from a dendritic shaft (d1). A TH-positive bouton (TH) makes symmetrical synaptic contact (arrows) with both the spine (s) and the dendritic shaft (d1) as well as neighboring dendritic shaft (d2). The latter also receives asymmetrical synaptic input (arrowheads) from a VGluT2-positive bouton (b2). D, VGluT2-positive bouton (b) makes asymmetrical synaptic contact (arrowhead) with a dendritic shaft (d) which is in symmetrical synaptic contact (arrow) with TH-positive terminal (TH). E, A VGluT2-positive bouton (b) makes asymmetrical synaptic contact (arrowheads) with a spine (s) which is synaptically contacted at its neck (symmetrical synapse: arrow) by a TH-positive terminal (TH). F, A VGluT2-positive bouton (b) makes asymmetrical synaptic contact (arrowheads) with a spine (s). A TH-positive terminal (TH) forms a symmetrical synapse (arrow) onto the opposite side of the same spine. The symmetrical synapses in this figure were identified by three criteria: a presynaptic accumulation of synaptic vesicles, synaptic cleft material and a darkened postsynaptic membrane (see Materials and Methods). Scale bars, 200 nm.
Figure 4.
TH-positive axons often appose VGluT1- and VGluT2-positive terminals. A, A TH-positive terminal (TH) is closely apposed (arrow) to a VGluT1-positive bouton (b), which in turn makes asymmetrical synaptic contact (arrowhead) with a spine (s). B, A TH-positive axon (TH) nestles at the edge of an asymmetrical synapse (arrowhead) between a VGluT1-positive bouton (b1) and a spine (s1). It is closely apposed (arrows) to b1, s1 and an additional spine, s2, which makes asymmetrical contact with an unlabeled bouton (b2). Scale bars, 200 nm.
Figure 5.
Schematic showing the proportions of VGluT1-positive (white numbers) or VGluT2-positive (black numbers) terminals (dark gray), their postsynaptic spines/shafts (light gray) and random control structures (black) that were apposed by TH-positive axons (white). Figures normalized for length of perimeter.
References
- Agnati LF, Zoli M, Strömberg I, Fuxe K. Intercellular communication in the brain: wiring versus volume transmission. Neuroscience. 1995;69:711–726. -PubMed
- Arbuthnott GW, Wickens J. Space, time and dopamine. Trends Neurosci. 2007;30:62–69. -PubMed
- Björklund A, Lindvall O. Dopamine-containing systems in the CNS. In: Björklund A, Hökfelt T, editors. Handbook of chemical neuroanatomy. Vol. 2. Amsterdam: Elsevier; 1984. pp. 55–122. Classical transmitters in the CNS Part 1.
- Bouyer JJ, Park DH, Joh TH, Pickel VM. Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res. 1984;302:267–275. -PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources