Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Stephenson-Jones, Marcus; Floros, Orestis; Robertson, Brita; Grillner, Sten

doi:10.1073/pnas.1119348109

Cited by 132 publications

(171 citation statements)

References 67 publications

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“…In one case, a modest increase in firing frequency occurred following TNPA application (0.5-0.85 Hz); in all other cases, the application of TNPA had no effect on the firing frequency, even after 20 min of drug application. In mammals and lamprey, the habenula-projecting pallidal neurons drive activity in the lateral habenula, which exerts an indirect inhibitory influence on dopamine neurons (12,26,27). Our results, therefore, show that dopamine projections back to the GPh close this loop and could form a positive-feedback circuit to regulate the dopaminergic system (Fig.…”

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

confidence: 79%

“…In mammals, the EPh exerts an excitatory influence on the lateral habenula (16), which, in turn, indirectly, via the rostromedial tegmental nucleus (RMTg), inhibits dopaminergic neurons in the VTA and SNc (15,17,27,41,42). The organization of the lateral habenula and its downstream targets is exceptionally well conserved (12). Consequently, changes in the firing rate of GPh neurons through activation of excitatory pallio-GPh and inhibitory striosome-GPh projections will lead to a decrease or increase in dopaminergic firing, respectively.…”

Section: Striosomal Inhibition Of Gph Decreases the Activity In Respomentioning

confidence: 99%

“…In this ancient vertebrate species, the habenula and thalamic/brainstem-projecting pallidal neurons are located in separate, nonoverlapping locations (11,12), which afford the possibility of untangling the circuitry that influences these separate populations.…”

mentioning

confidence: 99%

“…In addition to the output neurons that project to motor areas, a separate subpopulation of pallidal neurons projects to the lateral habenula (9)(10)(11)(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.…”

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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: 79%

Section: Striosomal Inhibition Of Gph Decreases the Activity In Respomentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

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 habenula (figure 1c) is an evolutionarily conserved structure in vertebrates [29]. It comprises two sub-nuclei-medial and lateral in mammals and dorsal and ventral in zebrafish Figure 1.…”

Section: (C) Habenula: the Dorsal Diencephalonmentioning

confidence: 99%

Zebrafish forebrain and temporal conditioning

Cheng

Jesuthasan

Penney

2014

Phil. Trans. R. Soc. B

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The rise of zebrafish as a neuroscience research model organism, in conjunction with recent progress in single-cell resolution whole-brain imaging of larval zebrafish, opens a new window of opportunity for research on interval timing. In this article, we review zebrafish neuroanatomy and neuromodulatory systems, with particular focus on identifying homologies between the zebrafish forebrain and the mammalian forebrain. The neuroanatomical and neurochemical basis of interval timing is summarized with emphasis on the potential of using zebrafish to reveal the neural circuits for interval timing. The behavioural repertoire of larval zebrafish is reviewed and we demonstrate that larval zebrafish are capable of expecting a stimulus at a precise time point with minimal training. In conclusion, we propose that interval timing research using zebrafish and whole-brain calcium imaging at single-cell resolution will contribute to our understanding of how timing and time perception originate in the vertebrate brain from the level of single cells to circuits.

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Brain Evolution and Comparative Neuroanatomy

Powers¹

2014

Encyclopedia of Life Sciences

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Brains have many diverse forms in different animal groups, from complex layered structures to simple nerve nets. The range of different brain forms is reflective of the huge variety of environmental niches and lifestyles in which organisms have been successful. Both simple and elaborate brains are adaptive, depending on the selective pressures to which organisms are subjected. In vertebrates, a basic plan can be recognised across groups, especially in the brainstem, but the forebrain of birds and mammals is much more elaborate than those of other vertebrates. Elaborate nervous systems have developed independently in some molluscs, arthropods and vertebrates. Correlated with this elaboration is the capacity for complex learning, which is highly developed in some molluscs, arthropods and birds and mammals. The presence of elaborated brains in disparate groups illustrates that evolution of the brain has not shown a trend from simple to complex, but rather has occurred independently in different lineages. Key Concepts: Two structures are homologous if they can be traced to a common ancestor. Because brains do not fossilise, establishment of brain homologies requires as much information as possible about the similarities between brains of different groups. There is no trend in the evolution of the brain. Specialisations in brain traits develop in response to the demands of various environmental selective pressures. Many animals with simple nervous systems are very successful. Two major groups of invertebrates can be distinguished: those with radial symmetry and those with bilateral symmetry. Those with radial symmetry have simple nervous systems with a ring of neurons, while bilaterally symmetrical organisms have concentrations of neurons in the head region. Octopi, insects and crustaceans have elaborate brains, well‐developed eyes and extensive learning ability, rivalling that of mammals. The brains of the earliest chordate ancestors of vertebrates had bilateral eyes, a diencephalon and hindbrain. All vertebrates have the same subdivisions of the brain: the hindbrain, midbrain and forebrain (the diencephalon and telencephalon). The hindbrain is relatively conservative, retaining a recognisable structure in spite of many variations, whereas the forebrain shows more variability among vertebrate groups. Twenty‐five cranial nerves can be recognised in vertebrates, innervating muscles of the head and specialized sense organs, including lateral line organs and taste buds on the body surface. The vertebrate telencephalon includes a dorsal pallial area which differentiates into the cerebral cortex in mammals, but there is disagreement about the homologous areas in nonmammals. Brains have evolved to enable organisms to compete successfully in different environmental niches and the adaptations they show reflect the demands of those environments.

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Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Cited by 132 publications

References 67 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

Zebrafish forebrain and temporal conditioning

Brain Evolution and Comparative Neuroanatomy

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