The Dopamine D2 Receptor Gene in Lamprey, Its Expression in the Striatum and Cellular Effects of D2 Receptor Activation

Robertson, Brita; Huerta-Ocampo, Icnelia; Ericsson, Johan; Stephenson-Jones, Marcus; Pérez‐Fernández, Juan; Bolam, J. Paul; Diaz-Heijtz, Rochellys; Grillner, Sten

doi:10.1371/journal.pone.0035642

Cited by 32 publications

(51 citation statements)

References 55 publications

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“…To determine how the dopaminergic innervation of the GPh affects neuronal firing, we first examined the dopamine receptor expression. In lamprey, dopamine D2 receptors are highly expressed in the striatum as well as in the GPh (25). In situ hybridization confirmed that neurons in the GPh express D2 receptor mRNA ( Fig.…”

Section: Direct Glutamatergic Projections From the Pallium (Cortex) Ementioning

confidence: 61%

“…Templates for in vitro transcription were prepared by PCR amplification. For the dopamine D2 receptor probe, a 660-bp fragment was obtained using 5′-TGCTCATATGCCTCATCGTC-3′ forward and 5′-TCAAGCTTTGCACAATCGTC-3′ reverse primers (25). The amplified cDNA fragments were cloned into a pCRII-TOPO vector (Invitrogen), cleaned, and confirmed by nucleotide sequencing (KIGene core facility at Karolinska Institutet).…”

Section: Methodsmentioning

confidence: 99%

“…In lamprey, as with other vertebrates, dopamine can cause a reduction in the excitability of neurons through activation of the D2 receptor (25). This suggested that activation of the GPh D2 receptors might lead to a decrease in the activity of the spontaneously active neurons.…”

Section: Direct Glutamatergic Projections From the Pallium (Cortex) Ementioning

confidence: 99%

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Independent circuits in the basal ganglia for the evaluation and selection of actions

Stephenson-Jones

Kardamakis

Robertson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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116

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The basal ganglia are critical for selecting actions and evaluating their outcome. Although the circuitry for selection is well understood, how these nuclei evaluate the outcome of actions is unknown. Here, we show in lamprey that a separate evaluation circuit, which regulates the habenula-projecting globus pallidus (GPh) neurons, exists within the basal ganglia. The GPh neurons are glutamatergic and can drive the activity of the lateral habenula, which, in turn, provides an indirect inhibitory influence on midbrain dopamine neurons. We show that GPh neurons receive inhibitory input from the striosomal compartment of the striatum. The striosomal input can reduce the excitatory drive to the lateral habenula and, consequently, decrease the inhibition onto the dopaminergic system. Dopaminergic neurons, in turn, provide feedback that inhibits the GPh. In addition, GPh neurons receive direct projections from the pallium (cortex in mammals), which can increase the GPh activity to drive the lateral habenula to increase the inhibition of the neuromodulatory systems. This circuitry, thus, differs markedly from the "direct" and "indirect" pathways that regulate the pallidal (e.g., globus pallidus) output nuclei involved in the control of motion. Our results show that a distinct reward-evaluation circuit exists within the basal ganglia, in parallel to the direct and indirect pathways, which select actions. Our results suggest that these circuits are part of the fundamental blueprint that all vertebrates use to select actions and evaluate their outcome.striosomes | reward/aversion | pallium/cortex | evolution T o achieve a goal, animals need to select actions and evaluate their outcome to determine whether their goal was achieved. In mammals, the basal ganglia play a key role in the selection of actions (1-3) and have more recently been suggested to additionally contribute to predicting and evaluating the outcome of the selected actions (4-8).The so-called "direct" and "indirect" pathways through the basal ganglia are present in all vertebrates and act together to select actions by decreasing tonic inhibition of the basal ganglia output nuclei [globus pallidus interna (GPi) and substantia nigra pars reticulata (SNr)] on a selected motor program and increasing the inhibition onto other competing actions. The output of these selection circuits target brainstem and thalamic motor areas, and neurons within this circuit are modulated by various aspect of movement kinetics related to the initiation and modulation of ongoing actions.In addition to the output neurons that project to motor areas, a separate subpopulation of pallidal neurons projects to the lateral habenula (9-12), a structure involved in evaluating and predicting the motivational value of actions. Recent in vivo recordings in primates have shown that the activity of these habenula-projecting pallidal neurons is modulated by the cues that predict the availability of reward (13,14) and not by aspects of movements. The majority of these pallidal neurons, as with latera...

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Section: Direct Glutamatergic Projections From the Pallium (Cortex) Ementioning

confidence: 61%

Section: Methodsmentioning

confidence: 99%

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Independent circuits in the basal ganglia for the evaluation and selection of actions

Stephenson-Jones

Kardamakis

Robertson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

116

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“…It has been widely used in lampreys, salamanders, rats, and human to label DA neurons (manufacturer's information) (22,28,(69)(70)(71)(72)(73). The 22941 TH antibody was used here on human tissue based on its successful use by Parent et al (74).…”

Section: Methodsmentioning

confidence: 99%

A descending dopamine pathway conserved from basal vertebrates to mammals

Ryczko

Cone

Alpert

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

104

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Dopamine neurons are classically known to modulate locomotion indirectly through ascending projections to the basal ganglia that project down to brainstem locomotor networks. Their loss in Parkinson's disease is devastating. In lampreys, we recently showed that brainstem networks also receive direct descending dopaminergic inputs that potentiate locomotor output. Here, we provide evidence that this descending dopaminergic pathway is conserved to higher vertebrates, including mammals. In salamanders, dopamine neurons projecting to the striatum or brainstem locomotor networks were partly intermingled. Stimulation of the dopaminergic region evoked dopamine release in brainstem locomotor networks and concurrent reticulospinal activity. In rats, some dopamine neurons projecting to the striatum also innervated the pedunculopontine nucleus, a known locomotor center, and stimulation of the dopaminergic region evoked pedunculopontine dopamine release in vivo. Finally, we found dopaminergic fibers in the human pedunculopontine nucleus. The conservation of a descending dopaminergic pathway across vertebrates warrants re-evaluating dopamine's role in locomotion.D opaminergic neurons represent a vital neuromodulatory component essential for vertebrate motor control, and their loss in neurodegenerative disease is devastating. The meso-diencephalic dopamine (DA) neurons are known to provide ascending projections to the basal ganglia, which, in turn, provide input to cortical structure in mammals but also project caudally to the mesencephalic locomotor region (MLR), a highly conserved structure that controls locomotion in all vertebrates investigated to date (1-7; for review, see ref. 8). A growing body of evidence supports the view that basal ganglia connectivity is highly conserved among vertebrates, from lampreys to mammals (9-11; for review, see ref. 12), with some interspecies differences recently highlighted (13). As such, the homology between DA cell populations remains to be resolved in vertebrates. As a general rule, DA neurons from the meso-diencephalon send projections to the striatum in all vertebrates. In lampreys and teleosts, those neurons are located only in the diencephalon (posterior tuberculum), but in tetrapods and cartilaginous fishes (14) they are located in both the diencephalon and the mesencephalon. An increasing number of authors seem to agree with the hypothesis that at least some of the mesodiencephalic DA neurons located in the diencephalon are homologous in all vertebrates, and thus, homologous to at least a portion of the mammalian substantia nigra pars compacta (SNc)/ ventral tegmental area (VTA) (13, 15-19; for review, see ref. 20). Alternatively, it was suggested that the posterior tuberculum DA neurons projecting to the striatum in zebrafish are homologs of the mammalian DA neurons of the A11 group (21). This will be discussed below in light of the results of the present study.In lampreys, only a few meso-diencephalic DA neurons send ascending projections to the striatum (9, 22); the majority ...

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“…Elements of this neuromodulatory organization may be conserved, because the striatum of non-mammalian vertebrates (lamprey, amphibians, reptiles, and birds) also receives a large dopaminergic projection from the homolog of the SNc/VTA and express D 1 and D 2 receptors (Reiner et al, 1998;Chu et al, 2001;Pombal et al, 2007;Robertson et al, 2012). Furthermore, in turtles and birds, dopamine excites striatal neurons that express D 1 receptors and inhibits neurons that express D 2 receptors (Ding and Perkel, 2002;Barral et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Dopamine Differentially Modulates the Excitability of Striatal Neurons of the Direct and Indirect Pathways in Lamprey

et al. 2013

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The functions of the basal ganglia are critically dependent on dopamine. In mammals, dopamine differentially modulates the excitability of the direct and indirect striatal projection neurons, and these populations selectively express dopamine D 1 and D 2 receptors, respectively. Although the detailed organization of the basal ganglia is conserved throughout the vertebrate phylum, it was unknown whether the differential dopamine modulation of the direct and indirect pathways is present in non-mammalian species. We aim here to determine whether the receptor expression and opposing dopaminergic modulation of the direct and indirect pathways is present in one of the phylogenetically oldest vertebrates, the river lamprey. Using in situ hybridization and patch-clamp recordings, we show that D 1 receptors are almost exclusively expressed in the striatal neurons projecting directly to the homolog of the substantia nigra pars reticulata. In addition, the majority of striatal neurons projecting to the homolog of the globus pallidus interna/globus pallidus externa express D 1 or D 2 receptors. As in mammals, application of dopamine receptor agonists differentially modulates the excitability of these neurons, increasing the excitability of the D 1 -expressing neurons and decreasing the excitability of D 2 -expressing neurons. Our results suggest that the segregated expression of the D 1 and D 2 receptors in the direct and indirect striatal projection neurons has been conserved across the vertebrate phylum. Because dopamine receptor agonists differentially modulate these pathways, increasing the excitability of the direct pathway and decreasing the excitability of the indirect pathway, this organization may be conserved as a mechanism that biases the networks toward action selection.

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The Dopamine D2 Receptor Gene in Lamprey, Its Expression in the Striatum and Cellular Effects of D2 Receptor Activation

Cited by 32 publications

References 55 publications

Independent circuits in the basal ganglia for the evaluation and selection of actions

Independent circuits in the basal ganglia for the evaluation and selection of actions

A descending dopamine pathway conserved from basal vertebrates to mammals

Dopamine Differentially Modulates the Excitability of Striatal Neurons of the Direct and Indirect Pathways in Lamprey

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