Activation of subthalamic neurons produces NMDA receptor-mediated dendritic dopamine release in substantia nigra pars reticulata: a microdialysis study in the rat

Rosales, Manuel G.; Flores, Gonzalo; Hernández, Salvador Villalpando; Martínez‐Fong, Daniel; Aceves, Jorge

doi:10.1016/0006-8993(94)91669-1

Cited by 62 publications

(38 citation statements)

References 19 publications

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“…The main input to the DA cells (either directly or indirectly) is from the striatum. Other sources of regulation of DA are derived from the globus pallidus (GP), the pedunculopontine n. (PPN), and the subthalamic n. (STN) (Carpenter et al, 1981a,b;Parent, 1986;Smith et al, 1990;Rosales et al, 1994;Charara et al, 1996;. Of these inputs, both the striatal and pallidal afferent fibers to the SN are GABAergic.…”

Section: Discussionmentioning

confidence: 99%

“…The cortico-STN projection, which has been a focus of study for motor and premotor cortico-basal ganglia system, is termed the 'hyperdirect' basal ganglia pathway in that impulses reach the basal ganglia output nuclei faster via this route than through the cortico-striatal pathway (Kolomiets et al, 2003). Given that the STN impacts directly on DA cells (Rosales et al, 1994;Meissner et al, 2003), this route (PFC to the STN to the midbrain cells) may represent an alternative in the primate to the direct PFC-VTA/SN pathway observed in other species. In fact, PFC stimulation results in both excitatory and inhibitory responses in the primate SN pars reticulata, which are mediated via the STN and striatum, respectively (Kitano et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

“…In fact, PFC stimulation results in both excitatory and inhibitory responses in the primate SN pars reticulata, which are mediated via the STN and striatum, respectively (Kitano et al, 1998). The PFC-STN connection in primates (Frankle et al, 2003), along with the direct STN connection to the SN, is likely to have an impact not only on the SN pars reticulata cells, but also on the DA neurons (Rosales et al, 1994). Figure 5 A schematic diagram of the ventral midbrain with a florescent photomicrograph from an individual case in which the anterograde tracer LY was placed in the prefrontal cortex.…”

Section: Discussionmentioning

confidence: 99%

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Prefrontal Cortical Projections to the Midbrain in Primates: Evidence for a Sparse Connection

Frankle

Laruelle

Haber

2006

Neuropsychopharmacol

117

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Frontal cortical efferent fibers are thought to have important regulatory influence on cortico-basal ganglia (BG) circuits. The corticomidbrain (substantia nigra/ventral tegmental area, SN/VTA) pathway has received particular attention in psychiatric diseases, most notably schizophrenia. Work in rodents demonstrates that the prefrontal cortico (PFC)-midbrain pathway plays a central role in regulating the firing pattern of dopamine (DA) neurons. These findings have led to some important hypotheses concerning PFC/BG interaction in schizophrenia. Descending PFC projections to the SN/VTA have been primarily documented in the rodent. The aim of this study was to determine the degree and organization of PFC afferents to these areas in the Macaque monkey. Anterograde tracer injections were made into discrete orbital, cingulate, and dorsolateral prefrontal areas. Projections were charted to the SN and VTA. Overall, there were very few fibers in the ventral midbrain following injections confined to specific areas of the PFC. To determine the relationship of the descending fibers to the midbrain DA neurons, sections were double stained for the tracer molecules and for tyrosine hydroxylase. In all cases, the prefrontal projections and the TH-positive cells did not appear to be in close juxtaposition. The results show a very limited projection from the PFC to the midbrain DA neurons in primates, terminating both within the SN proper as well as in the VTA. They arise from a broad region of the PFC, including the DLPF, cingulate, and orbital cortices. However, despite the relative lack of cortical input to the midbrain cells, these neurons are rich in glutamate receptors in primates. Thus, while, based on these anatomical studies, direct cortical control of DA neurons remains debatable in primates; the cortex may directly impact other sources of glutamatergic control.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Prefrontal Cortical Projections to the Midbrain in Primates: Evidence for a Sparse Connection

Frankle

Laruelle

Haber

2006

Neuropsychopharmacol

117

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“…Nevertheless, stimulation of the subthalamic nucleus has been shown to increase the release of dopamine in the SNr (Falkenburger et al 2001;Johnson et al 1992;Mintz et al 1986;Rosales et al 1994Rosales et al , 1997. Dopamine released in the SNr may in turn control presynaptic receptors at subthalamonigral (this work) and striatonigral terminals (Floran et al 1990;Radnikow and Misgeld 1998), thus controlling the activity of SNr neurons.…”

Section: Physiological Consequencesmentioning

confidence: 94%

“…This activity may induce a continuous excitation of SNr and SNc neurons. Continuous activation of dopaminergic neurons in the SNr or SNc (Iribe et al 1999;Kanazawa et al 1976) may produce a tonic extracellular level of dopamine in SNr (Falkenburger et al 2001;Mintz et al 1986;Richards et al 1997;Rohrbacher et al 2000;Rosales et al 1994Rosales et al , 1997. Accordingly, we explored whether dopamine receptors modulating subthalamonigral connections were partially active in the control (unstimulated) situation.…”

Section: Dopamine Receptors Can Be Tonically Activementioning

confidence: 99%

Control of the Subthalamic Innervation of Substantia Nigra Pars Reticulata by D₁ and D₂ Dopamine Receptors

Ibáñez-Sandoval

Hernández²,

Florán³

et al. 2006

Journal of Neurophysiology

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. Control of the subthalamic innervation of substantia nigra pars reticulata by D 1 and D 2 dopamine receptors. J Neurophysiol 95: 1800 -1811, 2006. First published November 23, 2005 doi:10.1152/jn.01074.2005. The effects of activating dopaminergic D 1 and D 2 class receptors of the subthalamic projections that innervate the pars reticulata of the subtantia nigra (SNr) were explored in slices of the rat brain using the whole cell patch-clamp technique. Excitatory postsynaptic currents (EPSCs) that could be blocked by 6-cyano-7-nitroquinoxalene-2,3-dione and D-(Ϫ)-2-amino-5-phosphonopentanoic acid were evoked onto reticulata GABAergic projection neurons by local field stimulation inside the subthalamic nucleus in the presence of bicuculline. Bath application of (RS)-2,3,4,5-tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine hydrochloride (SKF-38393), a dopaminergic D 1 -class receptor agonist, increased evoked EPSCs by ϳ30% whereas the D 2 -class receptor agonist, trans-(Ϫ)- 4aR-4,4a,5,6,7,8,8a,9-octahydro-5-propyl-1H-pyrazolo(3,4-g)quinoline (quinpirole), reduced EPSCs by ϳ25%. These apparently opposing actions were blocked by the specific D 1 -and D 2 -class receptor antagonists: R-(ϩ)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetra-hydro-1H-3-benzazepine hydrochloride (SCH 23390) and S-(Ϫ) -5-anino-sulfonyl-N-[(1-ethyl-2-pyrrolidinyl)-methyl]-2-methoxybenzamide (sulpiride), respectively. Both effects were accompanied by changes in the paired-pulse ratio, indicative of a presynaptic site of action. The presynaptic location of dopamine receptors at the subthalamonigral projections was confirmed by mean-variance analysis. The effects of both SKF-38393 and quinpirole could be observed on terminals contacting the same postsynaptic neuron. Sulpiride and SCH 23390 enhanced and reduced the evoked EPSC, respectively, suggesting a constitutive receptor activation probably arising from endogenous dopamine. These data suggest that dopamine presynaptically modulates the subthalamic projection that targets GABAergic neurons of the SNr. Implications of this modulation for basal ganglia function are discussed.

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Synaptic innervation of midbrain dopaminergic neurons by glutamate-enriched terminals in the squirrel monkey

1996

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The excitatory amino acid, glutamate, has long been thought to be a transmitter that plays a major role in the control of the firing pattern of midbrain dopaminergic neurons. The present study was aimed at elucidating the anatomical substrate that underlies the functional interaction between glutamatergic afferents and midbrain dopaminergic neurons in the squirrel monkey. To do this, we combined preembedding immunocytochemistry for tyrosine hydroxylase and calbindin D-28k with postembedding immunostaining for glutamate. On the basis of their ultrastructural features, three types (so-called types I, II, and III) of glutamate-enriched terminals were found to form asymmetric synapses with dendrites and perikarya of midbrain dopaminergic neurons. The type I terminals accounted for more than 70% of the total population of glutamate-enriched boutons in contact with dopaminergic cells in the dorsal and ventral tiers of the substantia nigra pars compacta as well as in the ventral tegmental area, whereas 5-20% of the glutamatergic synapses with dopaminergic neurons involved the two other types of terminals. The major finding of our study is that the glutamate-enriched boutons were involved in 70% of the axodendritic synapses in the ventral tegmental area. In contrast, less than 40% of the boutons in contact with dopaminergic dendrites were immunoreactive for glutamate in the dorsal and ventral tiers of the substantia nigra pars compacta. Approximately 50% of the terminals in contact with the perikarya of the different populations of midbrain dopaminergic neurons displayed glutamate immunoreactivity. In conclusion, our findings provide the first evidence that glutamate-enriched terminals form synapses with midbrain dopaminergic neurons in primates. The fact that the proportion of glutamatergic boutons in contact with dopaminergic cells is higher in the ventral tegmental area than in the substantia nigra pars compacta suggests that the different groups of midbrain dopaminergic neurons are modulated differently by extrinsic glutamatergic afferents in primates.

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Activation of subthalamic neurons produces NMDA receptor-mediated dendritic dopamine release in substantia nigra pars reticulata: a microdialysis study in the rat

Cited by 62 publications

References 19 publications

Prefrontal Cortical Projections to the Midbrain in Primates: Evidence for a Sparse Connection

Prefrontal Cortical Projections to the Midbrain in Primates: Evidence for a Sparse Connection

Control of the Subthalamic Innervation of Substantia Nigra Pars Reticulata by D₁ and D₂ Dopamine Receptors

Synaptic innervation of midbrain dopaminergic neurons by glutamate-enriched terminals in the squirrel monkey

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Activation of subthalamic neurons produces NMDA receptor-mediated dendritic dopamine release in substantia nigra pars reticulata: a microdialysis study in the rat

Cited by 62 publications

References 19 publications

Prefrontal Cortical Projections to the Midbrain in Primates: Evidence for a Sparse Connection

Prefrontal Cortical Projections to the Midbrain in Primates: Evidence for a Sparse Connection

Control of the Subthalamic Innervation of Substantia Nigra Pars Reticulata by D1 and D2 Dopamine Receptors

Synaptic innervation of midbrain dopaminergic neurons by glutamate-enriched terminals in the squirrel monkey

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Control of the Subthalamic Innervation of Substantia Nigra Pars Reticulata by D₁ and D₂ Dopamine Receptors