Effects of serotonin depletion on local interneurons in the developing olfactory pathway of lobsters

Benton, Jeanne L.; Beltz, Barbara S.

doi:10.1002/1097-4695(20010215)46:3<193::aid-neu1002>3.0.co;2-8

Cited by 35 publications

(19 citation statements)

References 53 publications

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“…One of our major interests is the serotonergic regulation of neurogenesis in the lobster brain. We have shown that serotonin levels regulate the rate of generation of new neurons in this system Benton and Beltz, 2001) and that neurogenesis is also under circadian control (Goergen et al, 2002). We hypothesized that if serotonin is involved in the circadian pathway that regulates neurogenesis, brain levels of this molecule should also cycle diurnally, be light entrainable and show a fixed relationship to the neurogenic rhythm.…”

Section: Discussionmentioning

confidence: 99%

“…are distinct, both regions nevertheless receive a massive serotonergic innervation from the same neuron -the ipsilateral dorsal giant neuron (DGN; Sandeman, 1987, 1994;Benton and Beltz, 2001). The input-output relationships of the DGN in these regions are not known, but in both regions this neuron innervates each and every glomerulus .…”

Section: Serotonergic Rhythms In the Olfactory And Accessory Lobesmentioning

confidence: 99%

“…In both vertebrate and invertebrate species, serotonin is a potent regulator of neurogenesis Daszuta, 1999, 2000;Benton and Beltz, 2001;Beltz et al, 2001;Jacobs, 2002;Radley and Jacobs, 2002;Malberg and Duman, 2003). In the brain of the American lobster, reduced serotonin levels result in a decrease in neurogenesis among the deutocerebral local and projection neurons (clusters 9 and 10; Fig.·1) Beltz et al, 2001), while elevated serotonin levels result in an increased rate of neurogenesis (J. L. Benton, E. M. Goergen and B. S. Beltz, unpublished results).…”

Section: Serotonin As a Regulator Of Neurogenesismentioning

confidence: 99%

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Regulation of serotonin levels by multiple light-entrainable endogenous rhythms

Wildt

Goergen

Benton

et al. 2004

Journal of Experimental Biology

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This study examined whether serotonin levels in the brain of the American lobster, Homarus americanus, are under circadian control. Using high-performance liquid chromatography and semi-quantitative immunocytochemical methods, we measured serotonin levels in the brains of lobsters at six time points during a 24-h period. Lobsters were maintained for 2·weeks on a 12·h:12·h light:dark cycle followed by 3·days of constant darkness. Under these conditions, brain serotonin levels varied rhythmically, with a peak before subjective dusk and a trough before subjective dawn. This persistent circadian rhythm in constant darkness indicates that serotonin levels are controlled by an endogenous clock. Animals exposed to a shifted light cycle for >10·days, followed by 3·days in constant darkness, demonstrate that this rhythm is light entrainable. Separate analyses of two pairs of large deutocerebral neuropils, the accessory and olfactory lobes, show that serotonin levels in these functionally distinct areas also exhibit circadian rhythms but that these rhythms are out of phase with one another. The olfactory and accessory lobe rhythms are also endogenous and light entrainable, suggesting the presence of multiple clock mechanisms regulating serotonin levels in different brain regions.

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Section: Discussionmentioning

confidence: 99%

Section: Serotonergic Rhythms In the Olfactory And Accessory Lobesmentioning

confidence: 99%

Section: Serotonin As a Regulator Of Neurogenesismentioning

confidence: 99%

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Regulation of serotonin levels by multiple light-entrainable endogenous rhythms

Wildt

Goergen

Benton

et al. 2004

Journal of Experimental Biology

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“…1 B and C). The DGNs have been the focus of extensive anatomical, physiological, and ultrastructural investigations because of their massive projections to the OLs and ALs where they innervate each and every glomerulus (16,(19)(20)(21)(22). The complex circuitry, sheer size, and geometry of the DGNs and their ubiquitous inputs throughout the OLs and ALs pose unusual challenges in understanding the function of the DGNs within the context of the olfactory system.…”

mentioning

confidence: 99%

“…Pharmacological depletion of serotonin during embryogenesis with 5,7-dihydroxytryptamine (5,7-DHT) dramatically reduces the size of the target neuropils of the DGN: the OL, AL, and OGTN (21,22). However, the morphology and size of the serotonergic DGNs are not affected by 5,7-DHT treatment (22).…”

mentioning

confidence: 99%

Transient uptake of serotonin by newborn olfactory projection neurons

Beltz

Benton

Sullivan

2001

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

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A life-long turnover of sensory and interneuronal populations has been documented in the olfactory pathways of both vertebrates and invertebrates, creating a situation where the axons of new afferent and interneuronal populations must insert into a highly specialized glomerular neuropil. A dense serotonergic innervation of the primary olfactory processing areas where these neurons synapse also is a consistent feature across species. Prior studies in lobsters have shown that serotonin promotes the branching of olfactory projection neurons. This paper presents evidence that serotonin also regulates the proliferation and survival of projection neurons in lobsters, and that the serotonergic effects are associated with a transient uptake of serotonin into newborn neurons.T he olfactory pathways of vertebrates and invertebrates show a remarkable degree of life-long structural plasticity. The basis of this plasticity is the turnover of olfactory receptor neurons (1, 2) as well as of interneuronal populations (3-5). The new afferents and interneurons insert their axons into existing synaptic regions, which are organized into a highly ordered array of glomeruli. These glomeruli are thought to be arranged odotopically, with each glomerulus having a specific role in the coding of odor quality (6-8). Throughout life, as the processes of new sensory neurons and interneurons are added to the glomeruli, their structural integrity is stable: there is no evidence for the formation of new glomeruli or the loss of existing glomeruli (9-11). The intercalation of the processes of new neurons into the glomeruli, in which pre-and postsynaptic populations of neurons need to be matched, presents major challenges for the nervous system in preserving odotopic order.A feature that is common to olfactory systems across phylogenetic lines is a dense serotonergic innervation of the regions where the olfactory receptor neurons synapse onto second-order cells. In vertebrates, the olfactory bulb is one of the major forebrain targets of serotonergic neurons ascending from the brainstem (12). In molluscs, serotonergic interneurons innervate the protocerebral olfactory neuropil where serotonin is thought to be involved in the storage of odor memory (13,14). Among the arthropods, giant serotonergic neurons innervate the antennal lobes of insects (15) and the olfactory lobes (OLs) of crustaceans (16). The present study examines the role this serotonergic innervation may play in the assembly and maintenance of olfactory areas in the lobster, Homarus americanus, by testing whether serotonin depletion influences the proliferation and survival of projection neurons and by documenting a transient uptake of serotonin by the newborn cells.The crustacean olfactory pathway consists of primary sensory neurons that synapse with local and projection interneurons within the glomeruli of the OLs. These two categories of interneurons are functionally analogous to the local (periglomerular and granule) and projection (mitral and tufted) neurons of the vertebrate olf...

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Neuromodulatory complement of the pericardial organs in the embryonic lobster, homarus americanus

Pulver

Marder

2002

J of Comparative Neurology

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The pericardial organs (POs) are a pair of neurosecretory organs that surround the crustacean heart and release neuromodulators into the hemolymph. In adult crustaceans, the POs are known to contain a wide array of peptide and amine modulators. However, little is known about the modulatory content of POs early in development. We characterize the morphology and modulatory content of pericardial organs in the embryonic lobster, Homarus americanus. The POs are well developed by midway through embryonic (E50) life and contain a wide array of neuromodulatory substances. Immunoreactivities to orcokinin, extended FLRFamide peptides, tyrosine hydroxylase, proctolin, allatostatin, serotonin, Cancer borealis tachykinin-related peptide, cholecystokinin, and crustacean cardioactive peptide are present in the POs by approximately midway through embryonic life. There are two classes of projection patterns to the POs. Immunoreactivities to orcokinin, extended FLRFamide peptides, and tyrosine hydroxylase project solely from the subesophageal ganglion (SEG), whereas the remaining modulators project from the SEG as well as from the thoracic ganglia. Double-labeling experiments with a subset of modulators did not reveal any colocalized peptides in the POs. These results suggest that the POs could be a major source of neuromodulators early in development.

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Effects of serotonin depletion on local interneurons in the developing olfactory pathway of lobsters

Cited by 35 publications

References 53 publications

Regulation of serotonin levels by multiple light-entrainable endogenous rhythms

Regulation of serotonin levels by multiple light-entrainable endogenous rhythms

Transient uptake of serotonin by newborn olfactory projection neurons

Neuromodulatory complement of the pericardial organs in the embryonic lobster, homarus americanus

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