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Parallel Medullary Gustatospinal Pathways in a Catfish: Possible

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Parallel Medullary Gustatospinal Pathways in a Catfish: Possible The Journal of Neuroscience, June 15, 1997, 17(12):4873–4885 Parallel Medullary Gustatospinal Pathways In a Catfish: Possible Neural Substrates for Taste-Mediated Food Search Jagmeet S. Kanwal and Thomas E. Finger Department of Cellular and Structural Biology, University of Colorado School of Medicine, 4200 East Ninth Avenue, Denver, Colorado 80262 Taste and tactile fibers in the facial nerve of catfish innervate of HRP or fluorescent tracers into the medial lobule of the FL extraoral taste buds and terminate somatotopically in the facial label a facioreticular projection terminating around the Rsps of lobe (FL)—a medullary structure crucial for gustatory-mediated RS5. DiI injections into this area of the RF retrogradely label food search. The present study was performed to determine deeply situated bipolar neurons, especially in the medial and the neural linkages between the gustatory input and the spinal intermediate lobules of the FL. Electrophysiological recordings motor output. Spinal injections of horseradish peroxidase in and around RS5 show units with large receptive fields and (HRP) label spinopetal cells in the octaval nuclei, the nucleus of with responses to chemical and tactile stimulation. The FL the medial longitudinal fasciculus, and reticulospinal neurons projects to the spinal cord via two pathways: (1) a topograph- (Rsps) in the brainstem medial reticular formation (RF), includ- ically organized direct faciospinal pathway, and (2) an indirect ing the Mauthner cell. A somatotopically organized, direct fa- facioreticulospinal pathway in which reticular neurons process ciospinal system originating from superficial cells scattered in and integrate gustatory information before influencing spinal the lateral lobule of the facial lobe (ll) is also labeled. The circuitry for motor control during food search. brainstem reticulospinal cells are segmentally organized into 14 clusters within eight segments of the reticular formation and Key words: facial lobe; nucleus of the solitary tract; reticular includes one cluster (RS5) directly ventral to the FL. Injections formation; taste; reticulospinal; feeding Many animal species possess elaborate sensory systems special- gustatory sense to detect and orient to chemical stimuli at a ized for locating food in their environment. For example, bats distance. Gustatory information must, therefore, reach motor use a highly developed audiovocal system to hunt insects via or premotor centers within the CNS to modulate orientation echolocation (Galambos, 1942; Griffin, 1958), toads have a and swimming, which are two essential behavioral components visual system specialized for detecting worm-like movements of food search. (Ewert, 1970), pit vipers use infrared receptors for tracking Previous anatomical studies (Herrick, 1905; Finger, 1978; their prey (Molenaar, 1974; Gruberg et al., 1979), and electric Morita and Finger, 1985) have established that the FL gives rise to fish use electroreception for detecting and locating food in three major projection systems: (1) an ascending lemniscal path- their environment (Bullock, 1982). Catfish have a highly sen- way reaching diencephalic levels directly and via a pontine relay, sitive, large gustatory sense that plays a critical role in the (2) a descending system ending in the funicular nuclei and spinal search for food in muddy waters (Herrick, 1901, 1904, 1905; cord (Sp) dorsal horn, and (3) local reflex connections to brain- Bardach et al., 1967; Atema, 1971; Caprio et al., 1993; Val- stem reticular formation. The ascending system does not reach the entincic and Caprio 1993). Catfish can detect concentration optic tectum (TeO), often a site of multimodal sensory integration differences between their maxillary barbels and make turning into a unified spatial map of the surroundings (Hartline et al., movements appropriate to locate food (Johnsen and Teeter, 1978; Knudsen, 1982). Although the FL maintains a highly or- 1980). The extraoral (facial nerve-innervated) taste receptors dered somatotopic map of gustatory space, this map is not re- are highly sensitive to amino acids (Caprio, 1975, 1978) and are tained in any of the higher lemniscal nuclei (Lamb and Caprio, mapped spatially within the facial lobe (FL), the primary gus- 1992; Lamb and Finger, 1996). Thus, spatial information about tatory nucleus for external taste (Finger, 1976; Marui and gustatory stimuli must be relayed to premotor centers from the FL Caprio 1982; Hayama and Caprio, 1989). Neuroethological and not from higher-order gustatory nuclei. studies show that the FLs are necessary for food localization The present study was initiated to identify premotor gustatory (Atema, 1971). These studies suggest that catfish use the facial centers and descending gustatomotor pathways in the channel catfish, Ictalurus punctatus. In an effort to localize these pathways, Received May 30, 1996; revised March 21, 1997; accepted April 7, 1997. we describe here the reticulospinal system, because it has not been This work was supported by National Institutes of Health Grant DC00147 (T.E.F.) and National Institutes of Health Training Grant T32 NS 07083. We thank Ba¨rbel described adequately in siluroid fishes. Electrophysiological inves- Bo¨ttger for technical help with many of the neuroanatomical procedures and Steve tigation of the relevant areas of the reticular formation were Singer for assistance in preparation of the electronic images. Correspondence should be addressed to Thomas E. Finger, Department of Cel- performed to determine whether neurons located there respond lular and Structural Biology, University of Colorado School of Medicine, 4200 East to chemical as well as tactile cues, and whether the receptive fields Ninth Avenue, Denver, CO 80262. of the reticular neurons are well defined and punctate as in the Jagmeet Kanwal’s present address: Department of Neurology, Georgetown Uni- versity Medical Center, 3970 Reservoir Road NW, Washington, DC 20007. FL, or relatively nonspecific and broad as in higher-order gusta- Copyright © 1997 Society for Neuroscience 0270-6474/97/174873-13$05.00/0 tory nuclei (Lamb and Caprio, 1993). 4874 J. Neurosci., June 15, 1997, 17(12):4873–4885 Kanwal and Finger • Gustatospinal Pathways in Catfish MATERIALS AND METHODS and FL. In one of these, two different fluorescent 10K dextran amines were used; in the other, biotinylated dextran was applied to the Sp and Animal acquisition and maintenance. Channel catfish, Ictalurus punctatus, HRP was applied to the FL. In the former case, fixation was with 4% (weighing 50–150 gm) were obtained from a local fish farm (Cline’s Trout paraformaldehyde in phosphate buffer and in the latter case, 2% para- Farm, Boulder, CO). The fish were maintained in aquaria kept at a 12 hr formaldehyde and 0.2% glutaraldehyde in buffer. The tissues were em- light/dark cycle. Animals were generally used for electrophysiological bedded in egg yolk, postfixed for an additional 2.5 hr, then transferred to studies within 2–3 weeks after being transported to laboratory aquaria. sucrose buffer for cryoprotection. The next day, 60 mm transverse sections Recordings from the reticular formation were obtained from .15 ani- were cut on a cryostat. mals. In a few cases, the recording was followed by iontophoretic injec- For dual fluorescence, the sections were mounted and coverslipped in tion of HRP at the recording site. All studies were approved by the fluoromount. For the biotin-HRP label, free-floating sections were re- University of Colorado Health Science Center Institutional Animal Use acted in a metal-intensified DAB solution containing 25 mg DAB, 20 mg and Care Committee. ammonium chloride, 0.5 ml of 1% cobalt chloride, 0.8 ml of 1% nickelous Neuroanatomical studies. Connections of the FL and reticular forma- ammonium sulfate, and 25 ml of glucose oxidase (Sigma Type V; 4 mg/ml tion (RF) were examined by the use of two in vivo tracers, HRP and in acetate buffer) in 50 ml of 0.1 M phosphate buffer. The reaction was dextran amines, and by postmortem diffusion of the carbocyanine dye, diI started with the addition of 2 ml of 1% b-D-glucose and monitored (1,19-dioctadecyl-3,3,39,39-tetramethylindocarbocyanine perchlorate). visually. This reaction produced a blue–black precipitate at the sites of Neuroanatomical results from in vivo tracer studies are based on horse- peroxidase activity. After completion of the reaction, the sections were radish peroxidase (HRP; Sigma, St. Louis, MO; Type VI) injections into rinsed in phosphate buffer and placed overnight in avidin–biotin complex the Sp of 12 animals and into the FL or reticular formation of 14 animals. in PBS plus 0.3% Triton X-100 per standard ABC protocols. The sections Formaldehyde-fixed brains of additional animals were used to obtain were reacted with nonintensified DAB (25 mg/50 ml buffer plus 30 mlof Nissl-stained sections in the transverse and horizontal planes for studying 3% hydrogen peroxide) the next day after rinsing in buffer, thereby the normal pattern of nuclear organization and for postmortem tracing. producing a brown reaction product at the sites of ABC binding. For postmortem studies, small crystals of diI were applied to the FL in Three-dimensional reconstruction of the reticulospinal system. Large uni- previously fixed (4% buffered paraformaldehyde) brains. After 2–8 lateral injections of HRP were made in the ventral horn of the Sp and the weeks, the tissue was sectioned on a vibratome and examined with a Zeiss tissue was processed for visualization of the labeled cells as explained in (Thornwood,
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