Spatial organization of olfactory receptor gene choice in the complete V1R-related ORA family of zebrafish

The vertebrate sense of smell employs four main receptor families for detection of odors, among them the V1R/ORA family, which is unusually small and highly conserved in teleost fish. Zebrafish possess just seven ORA receptors, enabling a comprehensive analysis of the expression patterns of the entire family. The olfactory organ of zebrafish is representative for teleosts, cup-shaped, with lamella covered with sensory epithelium protruding into the cup from a median raphe. We have performed quantitative in situ hybridization on complete series of horizontal cryostat sections of adult zebrafish olfactory organ, and have analysed the location of ora-expressing cells in three dimensions, radial diameter, laminar height, and height-within-the-organ. We report broadly overlapping, but distinctly different distributions for all ora genes, even for ora3a and ora3b, the most recent gene duplication. Preferred positions in different dimensions are independent of each other. This spatial logic is very similar to previous reports for the much larger families of odorant receptor (or) and V2R-related olfC genes in zebrafish. Preferred positions for ora genes tend to be more central and more apical than those we observed for these other two families, consistent with expression in non-canonical sensory neuron types

Lamprey possess both V1R and V2R olfactory receptors, but only V1Rs are expressed in olfactory sensory neurons

The sense of smell employs some of the largest gene families in the genome to detect and distinguish a multitude of different odors. Within vertebrates, 4 major olfactory receptor families have been described; of which, only 3 (OR, TAAR-like, and V1R) were found already in lamprey, a jawless vertebrate. The forth family (V2R) was believed to have originated later, in jawed vertebrates. Here we have delineated the entire vomeronasal receptor repertoire in 3 lamprey species. We report the presence of 6 v1r and 2 v2r genes in Lethenteron camtschaticum, arctic lamprey, and Lampetra fluviatilis, river lamprey (6 and 1, respectively, in sea lamprey, Petromyzon marinus). Three v1r genes but no v2r genes were found to be expressed in olfactory sensory neurons in the characteristic sparse expression pattern. Our results show the olfactory function of some V1Rs already in lamprey and, unexpectedly, an early origin of the V2R family in the shared ancestor of jawed and jawless vertebrates. However, lamprey v2r genes appear not to have acquired an olfactory function yet, thus dissociating the evolutionary origin of the family from the onset of a function as olfactory receptor

Spatial organization of olfactory receptor gene choice in the complete V1R-related ORA family of zebrafish

The vertebrate sense of smell employs four main receptor families for detection of odors, among them the V1R/ORA family, which is unusually small and highly conserved in teleost fish. Zebrafish possess just seven ORA receptors, enabling a comprehensive analysis of the expression patterns of the entire family. The olfactory organ of zebrafish is representative for teleosts, cup-shaped, with lamella covered with sensory epithelium protruding into the cup from a median raphe. We have performed quantitative in situ hybridization on complete series of horizontal cryostat sections of adult zebrafish olfactory organ, and have analysed the location of ora-expressing cells in three dimensions, radial diameter, laminar height, and height-within-the-organ. We report broadly overlapping, but distinctly different distributions for all ora genes, even for ora3a and ora3b, the most recent gene duplication. Preferred positions in different dimensions are independent of each other. This spatial logic is very similar to previous reports for the much larger families of odorant receptor (or) and V2R-related olfC genes in zebrafish. Preferred positions for ora genes tend to be more central and more apical than those we observed for these other two families, consistent with expression in non-canonical sensory neuron types

Individual Dopaminergic Neurons of Lamprey SNc/VTA Project to Both the Striatum and Optic Tectum but Restrict Co-release of Glutamate to Striatum Only

Dopaminergic neurons in the substantia nigra (SNc) innervate both striatum and the superior colliculus in mammals, as well as its homolog the optic tectum in lampreys, belonging to the oldest group of living verte-brates [1-3]. In the lamprey, we have previously shown that the same neuron sends axonal branches to both striatum and the optic tectum [3]. Here, we show that most neurons in the lamprey SNc and ventral tegmental area (VTA) (also referred to as the nucleus of the posterior tuberculum) express not only tyrosine hydroxylase (TH), in lamprey a marker of dopaminergic neurons [4], but also the vesicular glutamate transporter (vGluT), suggesting that glutamate is a co-transmitter. Remarkably, the axonal branches that project to striatum elicit both dopaminergic and glutamatergic synaptic effects on striatal neurons, whereas the axonal projections to the optic tectum only evoke dopaminergic effects. Thus, axonal branches from the same neuron can use two transmitters in one branch and only one in the other. Previous studies suggest that, along an individual dopaminergic axon, there can be microdomains of either TH or vGluT [5-8]. In addition, the present results demonstrate that entire axonal branches to one target structure can differ from that of branches to another target, both originating from the same dopamine neuron. This implies that a given dopamine neuron can exert different effects on two different target structures. The combined release of dopamine and glutamate may be appropriate in striatum, whereas the effects exerted on the tectal motor center may be better served with a selective dopaminergic modulation

Neuromodulation Can Be Simple: Myoinhibitory Peptide, Contained in Dedicated Regulatory Pathways, Is the Only Neurally-Mediated Peptide Modulator of Stick Insect Leg Muscle

In the best studied cases (Aplysia feeding, crustacean stomatogastric system), peptidergic modulation is mediated by large numbers of peptides. Furthermore, in Aplysia, excitatory motor neurons release the peptides, obligatorily coupling target activation and modulator release. Vertebrate nervous systems typically contain about a hundred peptide modulators. These data have created a belief that modulation is, in general, complex. The stick insect leg is a well-studied locomotory model system, and the complete stick insect neuropeptide inventory was recently described. We used multiple techniques to comprehensively examine stick insect leg peptidergic modulation. Single-cell mass spectrometry (MS) and immunohistochemistry showed that myoinhibitory peptide (MIP) is the only neuronal (as opposed to hemolymph-borne) peptide modulator of all leg muscles. Leg muscle excitatory motor neurons contained no neuropeptides. Only the common inhibitor (CI) and dorsal unpaired median (DUM) neuron groups, each neuron of which innervates a group of functionally-related leg muscles, contained MIP. We described MIP transport to, and receptor presence in, one leg muscle, the extensor tibiae (ExtTi). MIP application reduced ExtTi slow fiber force and shortening by about half, increasing the muscle's ability to contract and relax rapidly. These data show neuromodulation does not need to be complex. Excitation and modulation do not need to be obligatorily coupled (Aplysia feeding). Modulation does not need to involve large numbers of peptides, with the attendant possibility of combinatorial explosion (stomatogastric system). Modulation can be simple, mediated by dedicated regulatory neurons, each innervating a single group of functionally-related targets, and all using the same neuropeptide

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Additional file 5: of Overlapping but distinct topology for zebrafish V2R-like olfactory receptors reminiscent of odorant receptor spatial expression zones

Interspecies comparison of spatial expression patterns. Interspecies comparison of spatial distributions of several OR and V2R genes for adult zebrafish, larval Xenopus laevis, adult mouse and adult rat. The respective species is represented graphically, olfactory organ and the olfactory receptor gene family examined are noted below. The respective genes are indicated by color code, which is unique within each panel; gene names are as given in the respective publications. Spatial distributions are represented as ECDF (y axis). For the radial distribution, the x-axis represents the normalized radial distance with a scale ranging from 0 (central) to 1 (peripheral); for the height distribution the x-axis represents the normalized laminar height with a scale ranging from 0 (basal) to 1 (apical). For Xenopus V2R [25, 41] and zebrafish OR [10] the raw data of the respective publications were used to generate the graphs. Original gene names used in [10] were fZOR6 (or112–1), fZOR9 (or107–1), fZOR8 (or103–1), and fZOR5 (or102–1). Note the structural similarities between different species, olfactory organs, and olfactory receptor families. (PDF 557 kb