A Novel Neural Substrate for the Transformation of Olfactory Inputs into Motor Output

Derjean, Dominique; Moussaddy, Aimen; Atallah, Elias; St-Pierre, Melissa; Auclair, François; Chang, Steven L.; Ren, Xiang; Zielinski, Barbara S.; Dubuc, Réjean

doi:10.1371/journal.pbio.1000567

Cited by 72 publications

(128 citation statements)

References 49 publications

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“…In lampreys and salamanders, DA release in the MLR is concurrent with the activation of reticulospinal neurons, which trigger locomotion by transmitting the locomotor command caudally to spinal locomotor networks. In lampreys, the PT sends direct descending dopaminergic and glutamatergic inputs to the MLR (22,50). Importantly, in lampreys, pharmacological blockade of D1 receptors in the MLR dramatically decreased the duration of locomotor bouts, locomotor frequency, and the number of locomotor cycles elicited by PT stimulation (22).…”

Section: Discussionmentioning

confidence: 99%

“…Based on previous studies (4,7,50,80), the reticulospinal (RS) neurons were retrogradely labeled with the calcium (Ca 2+ ) indicator Ca 2+ green-dextran amines (MW 3000, Invitrogen C-6765) injected as crystals at the level of the first spinal segment, immediately after a complete transection. The preparation was then transferred for 18-24 h in a chamber perfused with cooled (8-10°C), oxygenated Ringer's solution to allow the tracer to migrate to fill the RS cell bodies.…”

Section: Methodsmentioning

confidence: 99%

“…Fast green was added to the solution for visualizing the injection site (e.g., refs. 7,22,37,50,58). The number of moles of ejected glutamate was estimated by measuring the volume of a droplet ejected in the air following a single pressure pulse multiplied by the number of pressure pulses (e.g., refs.…”

Section: Methodsmentioning

confidence: 99%

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A descending dopamine pathway conserved from basal vertebrates to mammals

Ryczko

Cone

Alpert

et al. 2016

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

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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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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

A descending dopamine pathway conserved from basal vertebrates to mammals

Ryczko

Cone

Alpert

et al. 2016

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

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104

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“…We find that the axons and their synaptic terminals of OB output neurons are closely associated with processes of dopaminergic neurons in the PT, rendering them a strong candidate for postsynaptic partner. Because a population of dopaminergic neurons in the PT send descending axons directly to the spinal cord 37 , it is conceivable that the OB-PT pathway may play general roles in olfaction such as evoking locomotion 47,48 . Further studies are required to precisely identify types of PT neurons connecting with the OB output neurons and to elucidate the functional aspects of this unique neural circuitry.…”

Section: Discussionmentioning

confidence: 99%

Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling

et al. 2014

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Chemotopic odour representations in the olfactory bulb are transferred to multiple forebrain areas and translated into appropriate output responses. However, a comprehensive projection map of bulbar output neurons at single-axon resolution is lacking in vertebrates. Here we unravel a projectome of the zebrafish olfactory bulb through genetic single-neuron tracing and image registration. We show that five major target regions receive distinct modes of projections from olfactory bulb glomeruli. The central portion of posterior telencephalon receives non-selective, interspersed inputs from all glomeruli, whereas the ventral telencephalon is diffusely innervated by axons from particular glomerular clusters. The right habenula and posterior tuberculum (diencephalic nuclei) receive convergent inputs from restricted and all glomerular clusters, respectively. The bulbar recurrent projections are coarsely topographic. Thus, the primary chemotopic organization is transformed into distinct sensory representations in higher olfactory centres. These findings provide a framework to understand general principles as well as species-specific features in decoding of odour information.

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“…In the olfactory bulb, the glomeruli receiving sensory inputs from the main olfactory epithelium are spatially segregated from that receiving accessory olfactory organ input. Olfactory sensory neurons in the main olfactory epithelium project to non-medial regions of the olfactory bulb (Ren et al, 2009) where output connects to the lateral pallium and extra pallial forebrain targets (Derjean et al, 2010;Green et al, 2013). A single glomerulus in the medial region of the olfactory bulb receives axons from olfactory sensory neurons located in the accessory olfactory organ (Ren et al, 2009) and medial projection neurons extend to the posterior tuberculum (Derjean et al, 2010;Green et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Odorant organization in the olfactory bulb of the sea lamprey

Green

Boyes

McFadden

et al. 2017

Journal of Experimental Biology

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Olfactory sensory neurons innervate the olfactory bulb, where responses to different odorants generate a chemotopic map of increased neural activity within different bulbar regions. In this study, insight into the basal pattern of neural organization of the vertebrate olfactory bulb was gained by investigating the lamprey. Retrograde labelling established that lateral and dorsal bulbar territories receive the axons of sensory neurons broadly distributed in the main olfactory epithelium and that the medial region receives sensory neuron input only from neurons projecting from the accessory olfactory organ. The response duration for local field potential recordings was similar in the lateral and dorsal regions, and both were longer than medial responses. All three regions responded to amino acid odorants. The dorsal and medial regions, but not the lateral region, responded to steroids. These findings show evidence for olfactory streams in the sea lamprey olfactory bulb: the lateral region responds to amino acids from sensory input in the main olfactory epithelium, the dorsal region responds to steroids (taurocholic acid and pheromones) and to amino acids from sensory input in the main olfactory epithelium, and the medial bulbar region responds to amino acids and steroids stimulating the accessory olfactory organ. These findings indicate that olfactory subsystems are present at the base of vertebrate evolution and that regionality in the lamprey olfactory bulb has some aspects previously seen in other vertebrate species.

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A Novel Neural Substrate for the Transformation of Olfactory Inputs into Motor Output

Abstract: Anatomical and physiological experiments in the lamprey reveal the neural circuit involved in transforming olfactory inputs into motor outputs, which was previously unknown in a vertebrate.

Cited by 72 publications

References 49 publications

A descending dopamine pathway conserved from basal vertebrates to mammals

A descending dopamine pathway conserved from basal vertebrates to mammals

Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling

Odorant organization in the olfactory bulb of the sea lamprey

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