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Olfactory Bulb Efferents in the Channel Catfish, Lctalurus Punctatus ANDREW H

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Olfactory Bulb Efferents in the Channel Catfish, Lctalurus Punctatus ANDREW H JOURNAL OF MORPHOLOGY 169:91-lll(1981) Olfactory Bulb Efferents in the Channel Catfish, lctalurus punctatus ANDREW H. BASS Division of Biological Sciences, Uniuersity of Michigan, Ann Arbor, Michigan 48109 ABSTRACT Autoradiographic, HRP, and Fink-Heimer techniques define ol- factory bulb efferents in the channel catfish. The olfactory bulb projects bilaterally to eight targets in the area ventralis telencephali including the preoptic area, five targets in area dorsalis telencephali, and the posterior tuber of the dience- phalon. There is additional input to the peripheral margin of the internal cell , layer of the contralateral olfactory bulb. Fibers cross in rostra1 (nervus terminalis and commissure of Goldstein) and caudal components of the anterior commissure and the habenular commissure. HRP techniques reveal the origin of bulb efferents from the internal and mitral cell layers of the olfactory bulb. The olfactory tract is divided into five major components, each with a unique subset of ipsilateral and commissural pathways. The actinopterygians, or ray-finned fishes, Braford, '80). (4) Comparable experimental are traditionally separated into three superor- data are available for a representative member ders (Romer, '701, namely the Chondrostei, of each of the other groups of actinopterygians Holostei, and Teleostei. The teleosts comprise (Braford and Northcutt, '74; Northcutt and at least 20,000 species and are further divided Braford, '80). into three divisions: I, the eels and eel-like This study is presented within the context fishes; 11, the mormyriforms and osteoglossi- of a cytoarchitectural analysis of the telence- forms; and 111, the bulk of teleost species phalon of the channel catfish, whose nomen- (Greenwood et al., '66). Teleosts display a wide clature is based on a series of normal and ex- range in variation of telencephalic organiza- perimental studies of several actinopterygians tion, which suggests that this is adapted to (Bass, '81a). This is the first experimental re- divergent ecological and behavioral niches. post that utilizes axonal transport methods to This study reveals the olfactory bulb effer- define olfactory bulb efferents in a nonmam- ents in a Division I11 teleost, the channel cat- malian vertebrate. The results offer new data fish, Zctalurus punctatus. The catfishes, order on: (a) the separate projections of the medial Siluriformes, form a major division (about 2,- and lateral olfactory tracts, (b) the number of 000 species) of the superorder Ostariophysi, olfactory bulb targets in the subpallium and which includes the majority of freshwater pallium, (c) olfactory bulb input to the preoptic fishes (5-6,000 species, Greenwood et al., '66). area and the contralateral olfactory bulb, and This demonstration of olfactory bulb efferents (d) the cells of origin of olfactory bulb efferents. is critical to understanding telencephalic or- A portion of these results appeared earlier ganization in catfish, and indeed, other teleosts (Bass, '78). for four reasons: (1) The early anatomists por- tray the telencephalon of teleosts as an olfac- MATERIALS AND METHODS tory-dominated structure (Johnston, '11; Her- rick, '21). (2) The olfactory system is the only Experimental animals sensory system with direct input to the telen- Adult and juvenile specimens of channel cat- cephalon. (3) It is impossible to correlate the fish, Ictalurus punctatus, were collected on the topography of telencephalic olfactory bulb tar- grounds of the Spring Valley Trout Farm, Dex- gets recognized in previous experimental stud- ter, Michigan. Animals were housed in aquaria ies (Scalia and Ebbesson, '71; Ito, '73; Finger, '75) with telencephalic subdivisions identified Andrew H. Bass's present address is Department of Ecology and in the majority of cytoarchitectural studies Behavioral Biology, 108 Zoology Building, 318 Church Street, S.E., (Nieuwenhuys, '63; Elass, '81a; Northcutt and Minneapolis, Minnesota 55455. 0362-2525/81/1691-0091$06.000 1981 ALAN R. LISS, INC. 92 A.H. BASS for at least 1 week prior to surgery, the water of the olfactory peduncle was transected prior temperature being maintained pre- and post- to injection of proline into the ipsilateral ol- operatively at 24-27°C. factory bulb (as above). These experiments were designed to elucidate the separate pro- Experimental methods jections of the medial (lateral transection) or Olfactory bulb efferents were traced by tran- lateral (medial transection) division of the ol- sections of the olfactory peduncle and olfactory factory tract. bulb injections of tritiated proline or horse- radish peroxidase (HRP). Prior to all surgical HRP injections procedures, animals were anesthetized by im- During a subsequent HRP analysis of olfac- mersion in home tank water containing tri- tory bulb afferents, anterograde transport of caine methanesulfonate (MS222). HRP (following olfactory bulb injections) con- firmed the trajectory of olfactory bulb effer- Transections ents. Experimental details appear elsewhere In four juvenile (18-10.5 cm, snout-tail (Bass, '81b). length) and four adult (27-28 cm) channel cat- For two juvenile (18-cm) channel catfish, the fish, the olfactory peduncle was transected ros- dorsal surface of the ipsilateral telencephalon tral to the anterior pole of the telencephalon. was exposed. The injection pipette was guided Following survival times of 1-12 days, animals stereotaxically into the rostromedial and cau- were anesthetized with MS222, and perfused dolateral segments of the hemisphere with transcardially with 0.7% saline followed by subsequent injections of 1.0-2.0 pl of HRP over 10%Formalin. All brains were fixed for at least a period of 5-10 min. These experiments were 1 week in 10% Formalin and were embedded designed to reveal the cells of origin of olfac- in 25% gelatin. Frozen sections were cut at 33 tory bulb efferents. Following reanesthetiza- bm in the transverse plane and stored in 2% tion with MS222, animals were perfused tran- Formalin. Sections were stained for degener- scardially with cold phosphate buffer (pH 7.4) ating axons and terminals according to the followed by 2% gluteraldehyde in cold buffer. Wiitanen modification of the Fink-Heimer After removal from the skull, each brain was technique (Wiitanen, '69). washed in 30% sucrose-fixative (2-3 hr) and then 30% sucrose-buffer (12 hr). Brains were Proline injections embedded in gelatin-sucrose and sectioned fro- Eight adult (28- to 42.5-cm) channel catfish zen at 33-40 pm. Staining procedures were received olfactory bulb injections of 0.1-0.5 pl modifications (cf. Bass, '79) of the O-dianisi- of tritiated proline (New England Nuclear dine reactions of Colman et al. ('76) and the NET-323, concentrated to 20 pCi/p,l). All in- tetramethylbenzidine (TMB) reaction of jections were made under pressure via a 1- DeOlmos et al. ('78). lambda pipette (drawn and bevelled to a tip of A distinct advantage of using catfish for the 75 p,m) attached to a stereotaxic device. Injec- study of olfactory bulb efferents with protein tions were made over a 5- to 10-min period. transport methods is that the olfactory bulb is Following postoperative survival times of 1-12 displaced from the rostra1 pole of the telence- days, animals were reanesthetized with phalon along extended olfactory peduncles MS222 and perfused transcardially, with 0.7% (Fig. 1).This condition alleviates the problem saline followed by AFA (see Bass, '81a). The of local diffusion of labeled protein into adja- brains were removed from the skull and placed cent structures (such as the telencephalon in in fixative for at least 1week, with subsequent animals with sessile bulbs), thus hindering the embedding in paraffin. Material was serially interpretation of pathways originating from sectioned at 15 pm, in either the transverse or the olfactory bulb. horizontal plane. The mounted sections were deparaffinized, coated with Kodak NTB2 or 3 RESULTS emulsion, and exposed at 7°C for 28 or 40 days. After development in D-19 or Dektol, sections Methodological notes were counterstained with cresyl violet. Trac- ings of high-contrast photographs from an ear- Silver degeneration lier cytoarchitectural study (Bass '81a) were Optimal terminal degeneration occurred in used to plot the distribution of silver grains. juvenile specimens (13-16 cm), surviving 5-7 In seven adult (31- to 37-cm) channel catfish, days at 26°C. By 9 or 10 days, argyrophilia was a portion of the medial and/or lateral division predominant in the olfactory tracts. Both ax- CATFISH OLFACTORY PATHWAYS 93 onal and terminal argyrophilic debris ap- Fibers appeared as sinuous lines of clumped peared as small- to medium-caliber black gran- reaction product oriented within the plane of ules (Fig. 9). In all cases, degeneration within section. Terminal zones contained a homoge- the lateral olfactory tract and the area dorsalis neous distribution of fine granular precipitate. telencephali was coarser and heavier than in Following telencephalic HRP injections, la- the medial olfactory tract and the area ven- beled cells within the olfactory bulb contain a tralis telencephali. Excepting the preoptic dense homogeneous and/or a granular precip- area, terminal debris occurred in all regions itate (Fig. 11). identified as targets with autoradiographic and HRP material. The trajectory of the medial Secondary olfactory pathways and terminal olfactory tract pars rnedialis could not be ac- fields: Overview curately traced with Fink-Heimer methods. The following description of olfactory bulb One bullhead
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