Summary
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1.
Electrophysiological responses to chemical stimuli were recorded from the spinal nerves innervating the free fin rays of the searobin,Prionotus carolinus. These modified pectoral fin rays are capable of detecting chemical stimuli although they contain neither taste buds nor olfactory receptors.
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2.
Squid extract elicited a vigorous response and of the 24 compounds which have been found in squid extract (Mackie 1982) 15 were tested. Ten of these compounds elicited increases in nerve activity and 5 were nonstimulatory (Table 1). Betaine (trimethylglycine) was the most stimulatory compound tested (Table 1) with a threshold of 10−6.2 mol/l.
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3.
Response magnitude increased with increasing concentration over approximately 2–3 log units for the most potent stimuli and saturated at higher concentrations (Figs. 4, 6).
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4.
Elimination of the methyl groups from betaine led to an increase in threshold concentration and a decrease in relative effectiveness. Substitution of a neutral hydroxymethyl group for the primary carboxyl group of betaine (choline) eliminated the response entirely (Table 1).
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5.
Single unit responses to chemical stimuli were similar to the multiunit integrated responses in terms of relative effectiveness, threshold, and concentration-response curves.
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6.
Vigorous responses to tactile and proprioceptive stimuli were obtained from all of the animals tested, indicating that the searobin fin rays are sensitive to mechanical as well as chemical stimulation.
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References
Alarie Y (1973) Sensory irritation of the upper airways by air-borne chemicals. Toxicol Appl Pharmacol 24:279–297
Anderson RK, Lund JP, Puil E (1978) Enkephalin and substance P effects related to trigeminal pain. Can J Physiol Pharmacol 56:216–222
Bardach JE, Case J (1965) Sensory capabilities of the modified fins of squirrel hake (Urophycis chuss) and sea robins (Prionotus carolinus andP. evolans). Copeia 2:194–206
Bardach J, Fujiya M, Holl A (1967a) Investigations of external chemoreceptors of fishes. In: Hayashi T (ed) Olfaction and taste II. Pergammon Press, New York, pp 647–655
Bardach J, Todd JH, Crickmer R (1967b) Orientation by taste in fish of the genusIctalurus. Science 155:1276–1278
Beidler LM (1954) A theory of taste stimulation. J Gen Physiol 38:133–139
Beidler LM (1965) Comparison of gustatory receptors, olfactory receptors, and free nerve endings. Cold Spring Harbor Symp Q Biol 30:191–200
Belghaug R, Døving KB (1977) Odour threshold determined by studies of the induced waves in the olfactory bulb of the char (Salmo alpinus). Comp Biochem Physiol A 57:327–330
Caprio J (1975) High sensitivity of catfish taste receptors to amino acids. Comp Biochem Physiol A 52:247–251
Caprio J (1978) Olfaction and taste in the channel catfish — Electrophysiological study of the response to amino acids and derivatives. J Comp Physiol 123:357–371
Caprio J (1980) Similarity of olfactory receptor responses (EOG) of freshwater and marine catfish to amino acids. Can J Zool 58:1778–1784
Caprio J (1982) High sensitivity and specificity of olfactory and gustatory receptors of catfish to amino acids. In: Hara TJ (ed) Chemoreception in fishes. Elsevier Sci Publ Co, Amsterdam, pp 109–134
Carr WES (1982) Chemical stimulation of feeding behavior. In: Hara TJ (ed) Chemoreception in fishes. Elsevier Sci Publ Co, Amsterdam, pp 259–273
Carr WES, Blumenthal KM, Netherton JC III (1977) Chemoreception in the pigfish,Orthopristis chrysopterus: the contribution of amino acids and betaine to stimulation of feeding behavior by various extracts. Comp Biochem Physiol A 58:69–73
Døving KB, Holmberg K (1974) A note on the function of the olfactory organ of the hagfish,Myxine glutinosa. Acta Physiol Scand 91:430–432
Finger TE (1982) Somatotopy in the representation of the pectoral fin and free fin rays in the spinal cord of the sea robin,Prionotus carolinus. Biol Bull 163:154–161
Goh Y, Tamura T (1980) Olfactory and gustatory responses to amino acids in two marine teleosts — red sea bream and mullet. Comp Biochem Physiol C 217–224
Hara TJ (1982) Structure-activity relationships of amino acids as olfactory stimuli. In: Hara TJ (ed) Chemoreception in fishes. Elsevier Sci Publ Co, Amsterdam, pp 135–157
Hara TJ, Carolina Law YM, Hobden BR (1973) Comparison of the olfactory response to amino acids in rainbow trout, brook trout, and white fish. Comp Biochem Physiol A 45:969–977
Herrick CJ (1904) The organ and sense of taste in fishes. Bull US Fish Commision for 1902. 22:237–272
Herrick CJ (1907) The tactile centers in the spinal cord of the brain of the sea robin,Prionotus carolinus L. J Comp Neurol 17:307–327
Hidaka I, Ohsugi T, Kubomatsu T (1978) Taste receptor stimulation and feeding behavior in the puffer,Fugu paradalis. I. Effect of single chemicals. Chem Senses Flav 3:341–354
Hokfelt T, Kellerth JO, Nilsson G, Pernow B (1975) Experimental immunohistochemical analysis on the localization and distribution of substance P in cat primary sensory neurons. Brain Res 100:235–252
Johnsen PB, Teeter JH (1980) Spatial gradient detection of chemical cues by catfish. J Comp Physiol 146:95–99
Kiyohara S, Tucker D (1978) Activity of new receptors after transection of the primary olfactory nerves. Physiol Behav 21:987–994
Kiyohara S, Hidaka T, Tamura T (1975) Gustatory response in the puffer. II. Single fiber analysis. Bull Jpn Soc Sci Fish 41:383–391
Kiyohara S, Yamashita S, Harada S (1981) High sensitivity of minnow gustatory receptors to amino acids. Physiol Behav 26:1103–1108
Lane EB, Whitear M (1982) Sensory structures at the surface of fish skin I. Putative chemoreceptors. Zool J Linn Soc 75:141–151
Lenhoff HM (1965) Some physicochemical aspects of the micro- and macroenvironments surrounding hydra during activation of their feeding behavior. Am Zool 5:515–524
Mackie AM (1982) Identification of gustatory feeding stimulants. In: Hara TJ (ed) Chemoreception in fishes. Elsevier Sci Publ Co., Amsterdam, pp 275–291
Morrill AD (1895) The pectoral appendages ofPrionotus and their innervation. J Morphol 11:177–192
Ohsugi T, Hidaka I, Ikeda M (1978) Taste receptor stimulation and feeding behavior in the puffer. II. Effects produced by mixtures of constituents of clam extracts. Chem Senses Flav 3:355–368
Parker GH (1912) The relations of smell, taste, and the common chemical sense in vertebrates. J Acad Natl Sci Philadelphia 18:221–234
Reutter K (1974) Cholinergic innervation of scattered sensory cells in fish epidermis. Cell Tissue Res 149:143–146
Scharrer E (1963) Intraepithelial nerve terminals in the free fin rays of the sea robin,Prionotus carolinus L. Anat Rec 145:367–368
Scharrer E, Smith SW, Palay SL (1947) Chemical sense and taste in the fishesPrionotus andTrichogaster. J Comp Neurol 86:183–193
Sheldon RE (1909) The reactions of the dogfish to chemical stimuli. J Comp Neurol Psychol 19:273–311
Silver WL (1979) Olfactory responses from a marine elasmobranch, the Atlantic stingray,Dasyatis sabina. Mar Behav Physiol 6:297–305
Silver WL (1982) Electrophysiological responses from the peripheral olfactory system of the American eel,Anguilla rostrata. J Comp Physiol 148:379–388
Silver WL, Maruniak JA (1981) Trigeminal chemoreception in the nasal and oral cavities. Chem Senses 6:295–305
Sutterlin AM, Sutterlin N (1970) Taste responses in Atlantic salmon (Salmo salar) parr. J Fish Res Bd Can 27:1927–1942
Sutterlin AM, Sutterlin N (1971) Electrical responses of the olfactory epithelium of Atlantic salmon (Salmo salar). J Fish Res Bd Can 28:565–572
Suzuki N (1978) Effects of different ionic environments on the responses of single olfactory receptors in the lamprey. Comp Biochem Physiol A 41:461–467
Suzuki N, Tucker D (1971) Amino acids as olfactory stimuli in freshwater catfish,Ictalurus catus (L.). Comp Biochem Physiol A 40:399–404
Tucker D (1963) Physical variables in the olfactory stimulation process. J Gen Physiol 46:453–489
Whitear M (1971) Cell specialization and sensory function in fish epidermis. J Zool 163:237–264
Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222
Yoshii K, Kamo N, Kurihara K, Kobatake Y (1979) Gustatory responses of eel palatine receptors to amino and carboxylic acids. J Gen Physiol 74:301–318
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Silver, W.L., Finger, T.E. Electrophysiological examination of a non-olfactory, non-gustatory chemosense in the searobin,Prionotus carolinus . J. Comp. Physiol. 154, 167–174 (1984). https://doi.org/10.1007/BF00604982
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DOI: https://doi.org/10.1007/BF00604982