Summary
-
1.
We examined the physiological properties and distribution of electroreceptors in the skin of adult lampreys (vertebrates, class: Agnatha) by recording electroreceptor afferent fiber activity in the anterior lateral line nerve. Stimulation was with uniform or local electric fields in the water around the fish.
-
2.
Lampreys possess ampullary electroreceptors widely distributed over the head and trunk (Fig. 1) that are sensitive to weak, low-frequency electric fields. The response thresholds to uniform fields are 1–10 μV/cm and the dynamic range of the receptors includes 4 log units of intensity (Fig. 3). Maximum sensitivity with sinusoidal currents is to frequencies ≦ 1 Hz (Fig. 4).
-
3.
Like the ampullary receptors of elasmobranchs and other non-teleost fishes, lamprey electroreceptors are excited by weak cathodal fields (i.e. negative at the receptor opening relative to a distant reference) and inhibited by anodal fields. With very intense stimuli (1–10 mV/cm) the responses reverse so that strong cathodal fields are inhibitory and anodal fields are excitatory (Fig. 3). These results indicate that similar transduction mechanisms exist in the electroreceptors of lampreys and non-teleost jawed fishes. Likewise, as in other non-teleosts, all electroreceptors in lampreys including those on the trunk are innervated by the anterior lateral line nerve.
-
4.
The similarities in receptor physiology and innervation taken in conjunction with known similarities in medullary organization indicate that electrosensory systems of lampreys and non-teleost gnathostome fishes are homologous.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- ALLN :
-
anterior lateral line nerve
- PLLN :
-
posterior lateral line nerve
References
Akoev GN, Ilyinsky OB, Zadan PM (1976) Physiological properties of electroreceptors of marine skates. Comp Biochem Physiol [A] 53:201–209
Bennett MVL (1971) Electroreception. In:Hoar WS, Randal DS (eds) Fish physiology. Academic Press, New York, pp 493–574
Berge JA (1979) The perception of weak electric AC currents by the European eel,Anguilla anguilla. Comp Biochem Physiol [A] 62:915–919
Bodznick DA, Northcutt RG (1980) Segregation of electro- and mechanoreceptive inputs to the elasmobranch medulla. Brain Res 195:313–321
Bodznick D, Northcutt RG (1981) Electroreception in lampreys; Evidence that the earliest vertebrates were electroreceptive. Science 212:465–467
Boord RL, Campbell CBG (1977) Structural and functional organization of the lateral line system of sharks. Am Zool 17:431–441
Bullock TH (1982) Electroreception. Annu Rev Neurosci 5:121–170
Bullock TH, Bodznick DA, Northcutt RG (1983) The phylogenetic distribution of electroreception: Evidence for convergent evolution of a sense modality. Brain Res Rev (in press)
Bullock TH, Northcutt RG, Bodznick DA (1982) Evolution of electroreception. Trends Neurosci 5:50–53
Clusin WT, Bennett MVL (1977a) Calcium-activated conductance in skate electroreceptors: current clamp experiments. J Gen Physiol 69:121–143
Clusin WT, Bennett MVL (1977b) Calcium-activated conductance in skate electroreceptors: voltage clamp experiments. J Gen Physiol 69:145–182
Enger PS, Kristensen L, Sand O (1976) The perception of weak electric DC currents by the European eel (Anguilla anguilla). Comp Biochem Physiol [A] 54:101–103
Fields RD, Lange DG (1980) Electroreception in the ratfish (Hydrolagus colliei). Science 207:547–548
Fritzsch B (1981a) The pattern of lateral-line afferents in urodeles. A horeseradish peroxidase study. Cell Tissue Res 218:581–594
Fritzsch B (1981b) Electroreceptors and direction specific arrangement in the lateral line system of salamanders. Z Naturforsch [C] 36:493–495
Hardisty MW (1979) Biology of the cyclostomes. Chapman and Hall, London
Himstedt W, Kopp J, Schmidt W (1982) Electroreception guides feeding behavior in amphibians. Naturwissenschaften 69:552–553
Johnston JB (1905) The cranial nerve components ofPetromyzon. Morphol Jahrb 34:149–203
Jørgensen JM (1980) The morphology of the Lorenzinian ampullae of the sturgeonAcipenser ruthenus (Pisces: Chondrostei). Acta Zool (Stockh) 61:87–92
Jørgensen JM, Flock A, Wersäll J (1972) The Lorenzinian ampullae ofPolyodon spathula. Z Zellforsch 130:362–377
Kalmijn AJ (1971) The electric sense of sharks and rays. J Exp Biol 55:371–383
Kalmijn AJ (1972) Bioelectric fields in sea water and the function of the ampullae of Lorenzini in elasmobranch fishes. Scripps Inst Oceanogr Ref Ser, pp 72–83
Kalmijn AJ (1974) The detection of electric fields from inanimate and animate sources other than electric organs. In: Fessard A (ed) Handbook of sensory physiology, vol III/3. Springer, Berlin Heidelberg New York, pp 147–200
Kleerekoper H, Sibakin K (1956a) An investigation of the electrical “spike” potentials produced by the sea lamprey (Petromyzon marinus) in the water surrounding the head region. J Fish Res Board Can 13:375–383
Kleerekoper H, Sibakin K (1956b) Spike potentials produced by the sea lamprey (Petromyzon marinus) in the water surrounding the head region. Nature 178:490–491
Kleerekoper H, Sibakin K (1957) An investigation of the electrical “spike” potentials produced by the sea lamprey (Petromyzon marinus) in the water surrounding the head region. II J Fish Res Board Can 14:145–151
Koester DM, Boord RL (1978) The central projections of first order anterior lateral line neurons of the clearnose skate,Raja eglanteria. Am Zool 18:587
McCormick CA (1982) The organization of the octavolateralis area in actinopterygian fishes: A new interpretation. J Morphol 171:159–181
Lindström T (1949) On the cranial nerves of the cyclostomes with special reference to n. trigeminus. Acta Zool (Stockh) 30:315–458
Moy-Thomas JA, Miles RS (1971) Palaeozoic fishes. Saunders, Philadelphia
Münz H, Claas B, Fritzsch B (1982) Electrophysiological evidence of electroreception in the axolotlSiredon mexicanum. Neurosci Lett 28:107–111
Murray RW (1962) The responses of the ampullae of Lorenzini of elasmobranchs to electrical stimulation. J Exp Biol 39:119–128
Northcutt RG (1980a) Central auditory pathways in anamniotic vertebrates. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, Berlin Heidelberg New York, pp 79–118
Northcutt RG (1980b) Anatomical evidence of electroreception in the coelacanth (Latimeria chalumnae). Zentralbl Veterinaer Med [C] 9:289–295
Northcutt RG, Bodznick DA, Bullock TH (1980) Most non- teleost fishes have electroreception. Proc Int Union Physiol Sci 14:614
Obara S, Bennett MVL (1972) Mode of operation of ampullae of Lorenzini of the skate,Raja. J Gen Physiol 60:534–557
Pearson AA (1936) The acoustico-lateral centers and the cerebellum, with fiber connections, of fishes. J Comp Neurol 65:201–294
Peters RC, Bretschneider F (1972) Electric phenomena in the habitat of the catfishIctalurus nebulosus LeS. J Comp Physiol 81:345–362
Pfeiffer W (1968) Die Fahrenholzschen Organe der Dipnoi und Brachiopterygii. Z Zellforsch 90:127–147
Randall DJ (1972) Respiration. In:Hardisty MW, Potter IC (eds) The biology of lampreys, vol 2. Academic Press, London, pp 287–306
Romer AS (1966) Vertebrate paleontology, 3rd edn. University of Chicago Press, Chicago
Rommel SA Jr, McCleave JD (1973) Sensitivity of American eels (Anguilla rostrata) and Atlantic salmon (Salmo salar) to weak electric and magnetic fields. J Fish Res Board Can 30:657–663
Roth A (1972) Wozu dienen die Elektrorezeptoren der Welse? J Comp Physiol 79:113–135
Roth A (1973) Electroreceptors in Brachiopterygii and Dipnoi. Naturwissenschaften 60:106–107
Roth A, Tscharntke H (1976) Ultrastructure of the ampullary electroreceptors in lungfish and Brachiopterygii. Cell Tissue Res 173:95–108
Rovainen CM (1974) Respiratory motoneurons in lampreys. J Comp Physiol 94:57–68
Rovainen CM (1977) Neural control of ventilation in the lamprey. Fed Proc 36:2386–2389
Royce WF, Smith S, Hartt AC (1968) Models of oceanic migrations of Pacific salmon and comments on guidance mechanisms. Fish Bull 66:441–462
Szabo T (1974) Anatomy of the specialized lateral line organs of electroreception. In: Fessard A (ed) Handbook of sensory physiology, vol III/3. Springer, Berlin Heidelberg New York, pp 13–58
Szamier RB, Bennett MVL (1980) Ampullary electroreceptors in the freshwater rayPotamotrygon. J Comp Physiol 138:225–230
Teeter JH, Szamier RB, Bennett MVL (1980) Ampullary electroreceptors in the sturgeonScaphirhyncus platorhyncus (Rafinesque). J Comp Physiol 138:213–223
Thomson KS (1977) On the individual history of cosmine and a possible electroreceptive function of the pore-canal system in fossil fishes. In: Andrews SM, Moles RS, Walker RD (eds) Problems in vertebrate evolution. Academic, New York, pp 247–271
Yamada Y (1973) Fine structure of the ordinary lateral line organ: I. The neuromast of lamprey,Entosphenus japonicus. J Ultrastruct Res 43:1–17
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bodznick, D., Preston, D.G. Physiological characterization of electroreceptors in the lampreysIchthyomyzon unicuspis andPetromyzon marinus . J. Comp. Physiol. 152, 209–217 (1983). https://doi.org/10.1007/BF00611185
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00611185