Abstract
BackgroundIn the olfactory system of malacostracan crustaceans, axonal input from olfactory receptor neurons associated with aesthetascs on the animal’s first pair of antennae target primary processing centers in the median brain, the olfactory lobes. The olfactory lobes are divided into cone-shaped synaptic areas, the olfactory glomeruli where afferents interact with local olfactory interneurons and olfactory projection neurons. The local olfactory interneurons display a large diversity of neurotransmitter phenotypes including biogenic amines and neuropeptides. Furthermore, the malacostracan olfactory glomeruli are regionalized into cap, subcap, and base regions and these compartments are defined by the projection patterns of the afferent olfactory receptor neurons, the local olfactory interneurons, and the olfactory projection neurons. We wanted to know how neurons expressing A-type allatostatins (A-ASTs; synonym dip-allatostatins) integrate into this system, a large family of neuropeptides that share the C-terminal motif –YXFGLamide.ResultsWe used an antiserum that was raised against the A-type Diploptera punctata (Dip)-allatostatin I to analyse the distribution of this peptide in the brain of a terrestrial hermit crab, Coenobita clypeatus (Anomura, Coenobitidae). Allatostatin A-like immunoreactivity (ASTir) was widely distributed in the animal’s brain, including the visual system, central complex and olfactory system. We focussed our analysis on the central olfactory pathway in which ASTir was abundant in the primary processing centers, the olfactory lobes, and also in the secondary centers, the hemiellipsoid bodies. In the olfactory lobes, we further explored the spatial relationship of olfactory interneurons with ASTir to interneurons that synthesize RFamide-like peptides. We found that these two peptides are present in distinct populations of local olfactory interneurons and that their synaptic fields within the olfactory glomeruli are also mostly distinct.ConclusionsWe discuss our findings against the background of the known neurotransmitter complexity in the crustacean olfactory pathway and summarize what is now about the neuronal connectivity in the olfactory glomeruli. A-type allatostatins, in addition to their localization in protocerebral brain areas, seem to be involved in modulating the olfactory signal at the level of the deutocerebrum. They contribute to the complex local circuits within the crustacean olfactory glomeruli the connectivity within which as yet is completely unclear. Because the glomeruli of C. clypeatus display a distinct pattern of regionalization, their olfactory systems form an ideal model to explore the functional relevance of glomerular compartments and diversity of local olfactory interneurons for olfactory processing in crustaceans.
Highlights
In the olfactory system of malacostracan crustaceans, axonal input from olfactory receptor neurons associated with aesthetascs on the animal’s first pair of antennae target primary processing centers in the median brain, the olfactory lobes
Because the glomeruli of C. clypeatus display a distinct pattern of regionalization, their olfactory systems form an ideal model to explore the functional relevance of glomerular compartments and diversity of local olfactory interneurons for olfactory processing in crustaceans
The olfactory interneurons are involved in modulation of olfactory processing and synthesize a vast variety of different neurotransmitters including serotonin, histamine and Gamma amino butyric acid (GABA) as well as many different neuropeptides such as RFamide related peptides, substance P, small cardiactive peptide b, orcokinins, SIFamide, and tachykinin-related peptides [10-18, review 19] In the present contribution we are interested in the distribution of the allatostatins in the brain, the central olfactory pathway, of a decapod crustacean, the hermit crab Coenobita clypeatus (Anomura, Coenobitidae) because these peptides previously had been shown to be abundant within the insect olfactory pathway [1]
Summary
In the olfactory system of malacostracan crustaceans, axonal input from olfactory receptor neurons associated with aesthetascs on the animal’s first pair of antennae target primary processing centers in the median brain, the olfactory lobes. The olfactory interneurons are involved in modulation of olfactory processing and synthesize a vast variety of different neurotransmitters including serotonin, histamine and GABA as well as many different neuropeptides such as RFamide related peptides, substance P, small cardiactive peptide b, orcokinins, SIFamide, and tachykinin-related peptides [10-18, review 19] In the present contribution we are interested in the distribution of the allatostatins in the brain, the central olfactory pathway, of a decapod crustacean, the hermit crab Coenobita clypeatus (Anomura, Coenobitidae) because these peptides previously had been shown to be abundant within the insect olfactory pathway [1]. The A-type allatostatins (A-ASTs; synonym dipallatostatins) constitute a large family of neuropeptides that were first identified from the cockroach Diploptera punctata and that share the C-terminal motif –YXFGLamide [reviews 1,20,21]. The family of crustacean A-ASTs has substantially grown to several dozens of representatives [6] with additional members being discovered in the prawns Penaeus monodon [24] and Macrobrachium rosenbergii [25], in the brachyuran crabs Cancer borealis [26] and Cancer productus [27], the crayfish Procambarus clarkii [17], the lobster Homarus americanus [4,28,29], the shrimps Litopenaeus vannamei [5] as well as a non-malacostracan crustacean, the copepod Calanus finmarchicus [30]
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