The olfactory epithelium of fish contains three intermingled types of olfactory receptor neurons (ORNs): ciliated, microvillous, and crypt. The present experiments were undertaken to test whether the different types of ORNs respond to different classes of odorants via different families of receptor molecules and G-proteins corresponding to the morphology of the ORN. In catfish, ciliated ORNs express OR-type receptors and Galpha(olf). Microvillous ORNs are heterogeneous, with many expressing Galpha(q)/11, whereas crypt ORNs express Galpha(o). Retrograde tracing experiments show that ciliated ORNs project predominantly to regions of the olfactory bulb (OB) that respond to bile salts (medial) and amino acids (ventral) (Nikonov and Caprio, 2001). In contrast, microvillous ORNs project almost entirely to the dorsal surface of the OB, where responses to nucleotides (posterior OB) and amino acids (anterior OB) predominate. These anatomical findings are consistent with our pharmacological results showing that forskolin (which interferes with Galpha(olf)/cAMP signaling) blocks responses to bile salts and markedly reduces responses to amino acids. Conversely, U-73122 and U-73343 (which interfere with Galpha(q)/11/phospholipase C signaling) diminish amino acid responses but leave bile salt and nucleotide responses essentially unchanged. In summary, our results indicate that bile salt odorants are detected predominantly by ciliated ORNs relying on the Galpha(olf)/cAMP transduction cascade. Nucleotides are detected by microvillous ORNs using neither Galpha(olf)/cAMP nor Galpha(q)/11/PLC cascades. Finally, amino acid odorants activate both ciliated and microvillous ORNs but via different transduction pathways in the two types of cells.
Extrinsic and intrinsic fiber connections of the telencephalic subdivisions of Nieuwenhuys ('62) in a teleost, Sebastiscus marmoratus, were studied by means of horseradish peroxidase (HRP) and Fink-Heimer methods. The olfactory bulb projects bilaterally to area dorsalis pars posterior, area ventralis pars ventralis, pars lateralis, pars posterior, pars intermedia, and the nucleus posterior tuberis of Peter et al. ('75) and receives fibers from ipsilateral area dorsalis pars centralis, pars posterior, area ventralis pars dorsalis, and pars supracommissuralis. Area dorsalis pars posterior sends numerous fibers to the ipsilateral ventral region of area dorsalis pars medialis, from which fibers of the medial forebrain bundle arise and terminate in the inferior lobe and nucleus posterior tuberis. Area dorsalis pars lateralis, pars dorsalis, and the dorsal region of pars medialis are the main targets of extratelencephalic ascending afferents. Area dorsalis pars lateralis receives fibers from the ipsilateral nucleus prethalamicus of Meader ('34), where tectal projections terminate massively. Area dorsalis pars dorsalis and the dorsal region of pars medialis receive afferents from the ipsilateral nucleus preglomerulosus of Schnitzlein ('62), nucleus posterior tuberis, area preoptica pars medialis of Crosby and Showers ('69), and nucleus entopeduncularis of Sheldon ('12). Raphe nuclei and locus ceruleus project bilaterally to area dorsalis pars centralis, pars dorsalis, pars lateralis, and the dorsal region of pars medialis. Area dorsalis pars centralis, pars dorsalis, and the dorsal region of pars medialis are important sources of extratelencephalic efferents. These subdivisions give rise to the lateral forebrain bundle and project to the ipsilateral nucleus prethalamicus, nucleus preglomerulosus, inferior lobe, nucleus paracommissuralis of Ito et al. ('82), optic tectum, torus semicircularis, and the bilateral mesencephalic tegmentum. Within the telencephalon, most of the ventral subdivisions project to ipsilateral area dorsalis pars centralis, pars dorsalis, pars lateralis, and the dorsal region of pars medialis. Area dorsalis pars centralis has reciprocal connections with ipsilateral area dorsalis pars lateralis, pars dorsalis, pars posterior, and the dorsal region of pars medialis. A dorsal part of the anterior commissure is composed of axons of the ventral region of area dorsalis pars medialis destined to the contralateral ventral region of area dorsalis pars medialis. A ventral part of the anterior commissure contains axons of area dorsalis pars centralis destined to contralateral area dorsalis pars lateralis.
The neuronal connections in the central gustatory system of the crucian carp were examined by means of degeneration and HRP methods. Cell morphology in the primary gustatory lobes was studied in Golgi-impregnated material. Medium-sized neurons of the facial lobe emit axons which project to the secondary gustatory nucleus. The nucleus intermedius facialis of Herrick ('05) projects bilaterally. Large neurons send axons through the spinal trigeminal tract to terminate in the spinal trigeminal nucleus and in the medial funicular nucleus. In the vagal lobe, second-order neurons for the ascending projections are located in the superficial part of the sensory zone. These neurons project exclusively to the ipsilateral secondary gustatory nucleus. Neurons located in the deeper part of the sensory zone send axons to the motor zone and to the brainstem reticular formation to form short reflex arcs. The glossopharyngeal lobe has similar neuronal connections to the vagal sensory zone. Both facial and vagal lobes receive afferent projections from the following central structures: nucleus posterioris thalami, nucleus diffusus lobi inferioris, optic tectum, motor nucleus of the trigeminal nerve, medullary reticular formation, and the gray matter of the upper spinal cord. The facial lobe has an additional afferent from the mesencephalic reticular formation. The major sources to the medullary gustatory lobes are the nucleus posterioris thalami and nucleus diffusus lobi inferioris. Each type of neuron classified by morphology and location in the facial, glossopharyngeal, and vagal lobes was correlated with its particular destination. Topographic projections were demonstrated in the secondary and tertiary gustatory centers.
The large majority of intraoral taste buds in goldfish are located on the gill arches and on the palatal organ, a muscular organ situated on the roof of the mouth. These taste buds are innervated by branches of the vagus nerve which terminate in a laminated vagal lobe, itself being an enlargement of the special visceral sensory column of the medulla. The tracer horseradish peroxidase (HRP) was used to determine the connectivity of the various branches of the vagus nerve that innervate the oropharyngeal gustatory surfaces. The entire oral cavity is mapped onto the vagal lobe so that the anterior end of the palatal organ and the most anterior gill arch are represented anteriorly in the vagal lobe; progressively more posterior oral structures are represented progressively more posteriorly in the lobe. The medial part of the palatal organ and the opposing gill arch surface, i.e., the ventromedial portion, are represented ventrally in the vagal lobe. The dorsolateral portions of the palatal organ and gill arches are represented dorsomedially in the vagal lobe. The topographic representation of the oral structures is similar for both the motor and sensory systems. In addition to this overall topographic organization, the different oropharyngeal structures are represented differentially in the layers of the vagal lobe. Palatal organ inputs reach layers VI and IX while gill arch inputs terminate in layers II, IV, and IX. The overall organization of the vagal lobe suggests a highly organized reflex system which is involved in the separation of food from substrate, especially during bottom feeding.
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