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Norekian, T. P.

Publications and source records attributed to Norekian, T. P..

11 recordsLinked to original sources

Glutamatergic system in the pelagic tunicates

Tunicates are a sister lineage to vertebrates, with compact, relatively simple nervous systems featuring a single central ganglion, reflecting a minimal complement of chordate functional architecture. Although glutamatergic neurons are the most abundant population in vertebrates, their ancestry remains unclear. Here, we used glutamate immunohistochemical labeling (Glutamate IR) to identify glutamatergic elements in the neural system of the pelagic tunicate Doliolum sp. (Thaliacea). Glutamate IR was observed in all major nerves of the central ganglion, including motor-like terminals on the circular bundles of swim muscles, which were themselves labeled. However, the neuronal somata in the central ganglion were not labeled, suggesting glutamate accumulation in axonal processes and terminals. In contrast, we did not identify GABA-containing neural elements. This study suggests that glutamatergic systems were elaborated in the common ancestor of tunicates and vertebrates, although the functional role of glutamate and its role in muscular control need further investigation in these pelagic tunicates.

zoology↗

Glutamatergic systems in Hydrozoa (Cnidaria)

The origins and early diversification of intercellular signaling molecules in animals remain poorly understood because comparative data across basal metazoan lineages are limited. Cnidarians form the sister group to bilaterian animals, and characterizing their transmitter systems is critical to understanding how complex adaptations within integrative systems shape evolutionary trajectories. Although glutamate is a well-established transmitter in bilaterian animals, its role in cnidarians remains unclear, and information on its neuronal function and signaling is limited. For most studied cnidarians, glutamate has been suggested to be a non-neuronal signaling molecule. Here, using glutamate immunoreactivity (Glu IR) in eight hydrozoan species with distinct ecologies (Aequorea victoria, Eutonina indicans, Clytia gregaria, Bougainvillia principis, Euphysa flammea, Polyorchis penicillatus, Aglantha digitalis, Nanomia septata), we identified and visualized distinct populations of glutamate-immunoreactive (Glu-ir) cells, including nematocytes, neurons, and muscle cells. A broad diversity of Glu-ir nematocytes was found in all studied species. Glu-ir neural cells were found only in three species (Aequorea, Nanomia, and Aglantha); their morphology and localization were species-specific. In addition, some striated and smooth myoepithelial cells were found to be either Glu-ir or GABA-ir. We propose that both glutamatergic and GABAergic systems were independently recruited more than 3 times as neurotransmitters across cnidarians, and that these recruitments are fundamentally rooted in bioenergetic demands.

evolutionary biology↗

Glutamatergic systems in ctenophores

Despite glutamates widespread role as the dominant excitatory transmitter in vertebrate brains, the early evolution of glutamate and its recruitment into neural signaling remain largely unknown. The major limitation is the lack of information on its distribution in early-branching basal metazoans, such as ctenophores (comb jellies). Here, using glutamate immunoreactivity (IR) in two ctenophore species with distinct ecologies (Pleurobrachia bachei and Beroe abyssicola), we show that glutamate IR is present in subpopulations of neurons within the subepithelial neural network and in small groups of mesogleal neuron-like cells, and that it differentially labels some muscle fibers. Remarkably, we also observed an enriched glutamate-ir signal within the nuclei of subepithelial neurons in Beroe. However, glutamate expression levels are species-specific, suggesting a tight coupling of glutamate recruitment for neural communication with energetic demands.

evolutionary biology↗

Neuromuscular Architecture of the Siphonophore Colony

Siphonophores are colonial hydrozoans with unprecedented differentiation and specialization, in which individual zooids are transformed into functional organs rather than autonomous polyps capable of feeding. As a result, the entire colony acts as a single, modular-individual with the highest level of coordination and integration, from development through behavior. Deciphering these integrative mechanisms requires understanding the microanatomical organization of the nervous system in all elements of the colony. Here, using two immunohistochemical markers (anti-tubulin and anti-RFamide antibodies), we systematically characterize the neural systems across the entire Nanomia colony, encompassing pneumatophore, stem and all zooid classes (nectophores, gastrozooids, palpons, male and female gonophores, and protective zooids). The use of two neuronal markers enables visualization of distinct neural subpopulations, some of which are not revealed by a single marker. We provide evidence of neuroanatomical interactions within all elements of the colony, including contributions of giant axons, stem polygonal networks, and RFamide-ir neural rings at the base of each zooid, as well as describe different subpopulations of neural networks in the body of various zooids. The presented mapping facilitates identification of novel conductive and signaling pathways for future analysis of the cellular basis of behavioral integration within decentralized, broadly distributed networks and non-neuronal elements of these unique superorganisms.

neuroscience↗

Structure and function of the nervous system in the stem of the siphonophore Nanomia septata: its role in swimming coordination.

The multiple swimming bells, or nectophores, of the colonial hydrozoan Nanomia septata are capable of coordinated avoidance swims in both forward and reverse directions. Individual nectophores also contribute to slower forms of swimming during foraging. Communication between a nectophore and the rest of the colony is at cone-shaped structures in the colonys stem. The stem provides an attachment point for the nectophores and houses the simple nervous system responsible for their coordination. The stem nervous system, revealed by immunocytochemistry, has three main components: two giant axons, a distributed, polygonal nerve network and a set of FMRFamide-immunoreactive nerve tracts. Whereas the nerve network is distributed throughout the stem, the nerve tracts link specific contra-lateral nectophores. Action potentials in the giant axons spread excitation rapidly along the stem, but their connection with individual nectophores is by way of the nerve network. Anatomical evidence is provided for the location of two connecting pathways between the nerve network and the nectophore; one excites an epithelial impulse and leads to reverse swimming; the other provides excitation for forward swimming by feeding into a ganglion-like cluster of nerve cells. Excitation passes to the swimming muscle epithelium by way of a single nerve axon and a nerve ring at the nectophore margin. The work presents physiological evidence for mechanisms, such as facilitation and summation, operating within a multifunctional, bidirectional nerve network, responsible for coordinating epithelial and neural signals in an early-evolved nervous system containing both condensed and distributed units. Summary statementHow a nervous system with two giant axons, a diffuse nerve network and FMRFamide-immunoreactive nerve tracts, coordinates Nanomias multiple swimming bells to provide the colony with foraging and escape behaviours.

neuroscience↗

Making Neurobots and Chimerical Ctenophores

Making living machines using biological materials (cells, tissues, and organs) is one of the challenges in developmental biology and modern biomedicine. Constraints in regeneration potential and immune self-defense mechanisms limit the progress in the field. Here, we present unanticipated features related to self-recognition and ancestral neuro-immune architectures of new emerging reference species - ctenophores or comb jellies. These are descendants of the earliest survival metazoan lineage with unique tissues, organs and independent origins of major animal traits such as neurons, muscles, mesoderm, and through-gut. Thus, ctenophores convergently evolved complex organization, compared to bilaterians. Nevertheless, their neural and immune systems are likely functionally coupled, enabling designs and experimental construction of hybrid neural systems and even entire animals. This report illustrates impressive opportunities to build both chimeric animals and neurobots using ctenophores as models for bioengineering. The obtained neurobots and chimeric animals from three ctenophore species (Bolinopsis, Mnemiopsis, and Pleurobrachia) were able to be autonomous and survive for days. In sum, the unification of biodiversity, cell biology, and neuroscience opens unprecedented opportunities for experimental synthetic biology.

developmental biology↗

The distribution and evolutionary dynamics of dopaminergic neurons in molluscs

Dopamine is one of the most versatile neurotransmitters in invertebrates. Its distribution and plethora of functions is likely coupled to feeding ecology, especially in Euthyneura (the largest clade of molluscs), which presents the broadest spectrum of environmental adaptations. Still, the analyses of dopamine-mediated signaling were dominated by studies of grazers. Here, we characterize the distribution of dopaminergic neurons in representatives of two distinct ecological groups: the sea angel - obligate predatory pelagic mollusc Clione limacina (Pteropoda, Gymnosomata) and its prey - the sea devil Limacina helicina (Pteropoda, Thecosomata) as well as the plankton eater Melibe leonina (Nudipleura, Nudibranchia). By using tyrosine hydroxylase-immunoreactivity (TH-ir) as a reporter, we showed that the dopaminergic system is moderately conservative among euthyneurans. Across all studied species, small numbers of dopaminergic neurons in the central ganglia contrast to significant diversification of TH-ir neurons in the peripheral nervous system, primarily representing sensory-like cells, which predominantly concentrated in the chemotactic areas and projecting afferent axons to the central nervous system. Combined with -tubulin immunoreactivity, this study illuminates the unprecedented complexity of peripheral neural systems in gastropod molluscs, with lineage-specific diversification of sensory and modulatory functions.

neuroscience↗

Structure and function of the nervous system in nectophores of the siphonophore Nanomia bijuga

O_LIAlthough Nanomia nectophores are specialized for locomotion, their cellular elements and complex nerve structures suggest they have multiple subsidiary functions. C_LIO_LIThe main nerve complex is a nerve ring, an adjacent columnar-shaped matrix plus two associated nerve projections. An upper nerve tract appears to provide a sensory input while a lower nerve tract connects with the rest of the colony. C_LIO_LIThe nerve cell cluster that gives rise to the lower nerve tract may relay information from the colony stem. C_LIO_LIThe structure of the extensively innervated "flask cells" located around the bell margin suggests a secretory function. They are ideally placed to release chemical messengers or toxins into the jet of water that leaves the nectophore during each swim. C_LIO_LIThe numerous nematocytes present on exposed nectophore ridges appear to have an entangling rather than a penetrating role. C_LIO_LIMovements of the velum, produced by contraction of the Claus muscle system during backwards swimming, can be elicited by electrical stimulation of the surface epithelium even when the major nerve tracts serving the nerve ring have been destroyed (confirming Mackie, 1964). C_LIO_LIEpithelial impulses generated by electrical stimulation elicit synaptic potentials in Claus muscle fibres. Their amplitude suggests a neural input in the vicinity of the Claus muscle system. The synaptic delay is <1.3 ms (Temperature 11.5 to 15{degrees} C). C_LIO_LIDuring backward swimming radial muscle fibres in the endoderm contract isometrically providing the Claus fibres with a firm foundation. C_LI Summary StatementNanomia colonies have specialized swimming bells capable of backwards swimming; thrust is redirected by an epithelial signal that leads to muscle contraction via a synaptic rather than an electrotonic event.

neuroscience↗

Comparative single-cell transcriptomics of complete insect nervous systems

Molecular profiles of neurons influence information processing, but bridging the gap between genes, circuits, and behavior has been very difficult. Furthermore, the behavioral state of an animal continuously changes across development and as a result of sensory experience. How behavioral state influences molecular cell state is poorly understood. Here we present a complete atlas of the Drosophila larval central nervous system composed of over 200,000 single cells across four developmental stages. We develop polyseq, a python package, to perform cell-type analyses. We use single-molecule RNA-FISH to validate our scRNAseq findings. To investigate how internal state affects cell state, we optogentically altered internal state with high-throughput behavior protocols designed to mimic wasp sting and over activation of the memory system. We found nervous system-wide and neuron-specific gene expression changes. This resource is valuable for developmental biology and neuroscience, and it advances our understanding of how genes, neurons, and circuits generate behavior.

neuroscience↗

Neural System and Receptor Diversity in the ctenophore Beroe abyssicola

Although, neuro-sensory systems might evolve independently in ctenophores, very little is known about their neural organization. Most of the ctenophores are pelagic and deep-water species and cannot be bred in the laboratory. Thus, it is not surprising that neuroanatomical data are available for only one genus within the group - Pleurobrachia. Here, using immunohistochemistry and scanning electron microscopy, we describe the organization of two distinct neural subsystems (subepithelial and mesogleal) and the structure of different receptor types in the comb jelly Beroe abyssicola - the voracious predator from North Pacific. A complex subepithelial neural network of Beroe, with five receptor types, covers the entire body surface and expands deeply into the pharynx. Three types of mesogleal neurons are comparable to the cydippid Pleurobrachia. The predatory lifestyle of Beroe is supported by the extensive development of ciliated and muscular structures including the presence of giant muscles and feeding macrocilia. The obtained neuroanatomy atlas provides unique examples of lineage-specific innovations within these enigmatic marine animals, and remarkable complexity of sensory and effector systems in this clade of basal Metazoa.\n\nGraphical AbstractAlthough, neuro-sensory systems might evolve independently in ctenophores, very little is known about their neuroanatomy. Here, using immunohistochemistry and scanning electron microscopy, we describe the organization of two neural systems and five different receptor types in the comb jelly Beroe abyssicola - the voracious predator from North Pacific. The predatory lifestyle of Beroe is supported by the extensive development of ciliated, muscular, and nervous systems including the presence of giant muscles and exceptional feeding macrocilia. The obtained neuroanatomy atlas provides unique examples of lineage-specific innovations within this enigmatic group of marine animals.\n\n\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=150 SRC=\"FIGDIR/small/419218_figG.gif\" ALT=\"Figure 1\">\nView larger version (94K):\norg.highwire.dtl.DTLVardef@1ce7930org.highwire.dtl.DTLVardef@766e6dorg.highwire.dtl.DTLVardef@14bc5baorg.highwire.dtl.DTLVardef@1a27072_HPS_FORMAT_FIGEXP M_FIG C_FIG

evolutionary biology↗

Atlas of Neuromuscular Organization in the Ctenophore, Pleurobrachia bachei (A. Agassiz, 1860)

Enigmatic ctenophores are descendants of one of the earliest branching metazoan lineage. Their nervous systems are equally elusive. The lack of convenient neurogenic molecules and neurotransmitters suggests an extensive parallel evolution and independent origins of neurons and synapses. However, the field is logged behind due to the lack of microanatomical data about the neuro-muscular systems in this group of animals. Here, using immunohistochemistry and scanning electron microscopy, we describe the organization of both muscular and nervous systems in the sea gooseberry, Pleurobrachia bachei, from North Pacific. The diffused neural system of Pleurobrachia consists of two subsystems: the subepithelial neural network and the mesogleal net with about 5000-7000 neurons combined. Our data revealed the unprecedented complexity of neuromuscular organization in this basal metazoan lineage. The anatomical diversity of cell types includes at least nine broad categories of neurons, five families of surface receptors and more than two dozen types of muscle cells as well as regional concentrations of neuronal elements to support ctenophore feeding, complex swimming, escape and prey capture behaviors. In summary, we recognize more than 80 total morphological cell types. Thus, in terms of cell type specification and diversity, ctenophores significantly exceed what we currently know about other prebilaterian groups (placozoan, sponges, and cnidarians), and some basal bilaterians.\n\n\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=150 SRC=\"FIGDIR/small/385435_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (114K):\norg.highwire.dtl.DTLVardef@151a0f4org.highwire.dtl.DTLVardef@1e0b71org.highwire.dtl.DTLVardef@813415org.highwire.dtl.DTLVardef@827e25_HPS_FORMAT_FIGEXP M_FIG C_FIG

evolutionary biology↗