Skip to main content
SpringerLink
Log in

Physiology of Tuberous Electrosensory Systems

  • Chapter
Electroreception

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 21))

5. Summary

Tuberous electrosensory system has two major behavioral functions, electrolocation and electrocommunication, which are unique to gymnotiform and mormyriform electric fishes that emit EODs with high-frequency components. This chapter presented an abundance of information about how peripheral and central physiological mechanisms carry out these behavioral functions. Electrolocation involves identification of stimulus features such as location (direction and distance), size, and electrical properties (resistance and capacitance) of objects. These features are detected and analyzed by two separate tuberous pathways specialized for amplitude and time processing. The parallel processing of amplitude and time in the hindbrain converges in the midbrain to produce neurons with more complex response properties. Electrocommunication for sex recognition in pulse-type mormyriforms relies on time-coding of waveform (pulse duration) of their EODs. Pulse duration is sampled by a type of time-coding electroreceptors (knollenorgan) that are specialized for communication and is decoded in the midbrain.

Understanding of the tuberous electrosensory system of electric fishes has been greatly advanced as a result of the interdisciplinary approach involving ethological, anatomical, physiological, and computational methods. Future studies with these methods should continue to provide complementary data for better understanding of behavioral mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Amagai S (1998) Time coding in the midbrain of mormyrid electric fish. II. Stimulus selectivity in the nucleus exterolateralis pars posterior. J Comp Physiol A 182:131–143.

    Article  PubMed  CAS  Google Scholar 

  • Amagai S, Friedman MA, Hopkins CD (1998) Time coding in the midbrain of mormyrid electric fish. I. Physiology and anatomy of cells in the nucleus exterolateralis pars anterior. J Comp Physiol 182:115–130.

    Article  CAS  Google Scholar 

  • Art JJ, Fettiplace R, Wu YC (1993) The effects of low calcium on the voltage-dependent conductances involved in tuning of turtle hair cells. J Physiol 470:109–126.

    PubMed  CAS  Google Scholar 

  • Bass AH, Hopkins CD (1982) Comparative aspects of brain organization of an African “wave” electric fish, Gymnarchus niloticus. J Morphol 174:313–334

    Article  Google Scholar 

  • Bass AH, Hopkins CD (1984) Shifts in frequency tuning of electroreceptors in androgentreated mormyrid fish. J Comp Physiol 155:713–724.

    Article  CAS  Google Scholar 

  • Bastian J (1976) Frequency response characteristics of electroreceptors in weakly electric fish (Gymnotoidei) with a pulse discharge. J Comp Physiol 112:165–180.

    Article  Google Scholar 

  • Bastian J (1977) Variations in the frequency response of electroreceptors dependent on receptor location in weakly electric fish (Gymnotoidei) with a pulse discharge. J Comp Physiol 121:53–64.

    Article  Google Scholar 

  • Bastian J (1981a) Electrolocation. I. How the electroreceptors of Apteronotus lbifrons code for moving objects and other electrical stimuli. J Comp Physiol 144:465–479.

    Article  Google Scholar 

  • Bastian J (1981b) Electrolocation. II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus albifrons. J Comp Physiol 144:481–494.

    Article  Google Scholar 

  • Bastian J (1986a) Electrolocation. Behavior, anatomy, and physiology. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 577–612.

    Google Scholar 

  • Bastian J (1986b) Gain control in the electrosensory system: a role for the descending projections to the electrosensory lateral line lobe. J Comp Physiol 158:505–515.

    Article  CAS  Google Scholar 

  • Bastian J (1986c) Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe. J Neurosci 6:553–562.

    PubMed  CAS  Google Scholar 

  • Bastian J (1996a) Plasticity in an electrosensory system. I. General features of a dynamic sensory filter. J Neurophysiol 76:2483–2496.

    PubMed  CAS  Google Scholar 

  • Bastian J (1996b) Plasticity in an electrosensory system. II. Postsynaptic events ssociated with a dynamic sensory filter. J Neurophysiol 76:2497–2507.

    PubMed  CAS  Google Scholar 

  • Bastian J (1998) Plasticity in an electrosensory system. III. Contrasting properties of spatially segregated dendritic inputs. J Neurophysiol 79:1839–1857.

    PubMed  CAS  Google Scholar 

  • Bastian J, Bratton B (1990) Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe. J Neurosci 10:1226–1240.

    PubMed  CAS  Google Scholar 

  • Bastian J, Heiligenberg W (1980a) Neural correlates of the jamming avoidance response in Eigenmannia. J Comp Physiol 136:135–152.

    Article  Google Scholar 

  • Bastian J, Heiligenberg W (1980b) Phase-sensitive midbrain neurons in Eigenmannia: neural correlates of the jamming avoidance response. Science 209:828–831.

    PubMed  CAS  Google Scholar 

  • Bastian J, Nguyenkim J (2001) Dendritic modulation of burst-like firing in sensory eurons. J Neurophysiol 85:10–22.

    PubMed  CAS  Google Scholar 

  • Bastian J, Chacron MJ, Maler L (2002) Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22:4577–4590.

    PubMed  CAS  Google Scholar 

  • Bell CC (1981) An efference copy which is modified by reafferent input. Science 214: 450–452.

    PubMed  CAS  Google Scholar 

  • Bell CC (1990) Mormyromast electroreceptor organs and their afferent fibers in ormyrid fish. III. Physiological differences between two morphological types of fibers. J Neurophysiol 63:319–332.

    PubMed  CAS  Google Scholar 

  • Bell CC, Grant K (1989) Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish. J Neurosci 9:1029–1044.

    PubMed  CAS  Google Scholar 

  • Bell CC, Russell CJ (1978) Effect of electric organ discharge on ampullary receptors in a mormyrid. Brain Res 145:85–96.

    Article  PubMed  CAS  Google Scholar 

  • Bell CC, von der Emde G (1995) Electric organ corollary discharge pathways in ormyrid fish: II. The medial juxtalobar nucleus. J Comp Physiol 177:463–479.

    Google Scholar 

  • Bell CC, Finger TE, Russell CJ (1981) Central connections of the posterior lateral line lobe in mormyrid fish. Exp Brain Res 42:9–22.

    Article  PubMed  CAS  Google Scholar 

  • Bell CC, Libouban S, Szabo T (1983) Pathways of the electric organ discharge command and its corollary discharges in mormyrid fish. J Comp Neurol 216:327–338.

    Article  PubMed  CAS  Google Scholar 

  • Bell CC, Zakon H, Finger TE (1989) Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish: I. Morphology. J Comp Neurol 286:391–407.

    Article  PubMed  CAS  Google Scholar 

  • Bell CC, Grant K, Serrier J (1992) Sensory processing and corollary discharge effects in the mormyromast regions of the mormyrid electrosensory lobe. I. Field potentials, cellular activity in associated structures. J Neurophysiol 68:843–858.

    PubMed  CAS  Google Scholar 

  • Bell CC, Dunn K, Hall C, Capti A (1995) Electric organ corollary discharge pathways in mormyrid fish. I. The mesencephalic command associated nucleus. J Comp Physiol 177:449–462.

    Google Scholar 

  • Bell CC, Han VZ, Sugawara Y, Grant K (1997) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387:278–281.

    Article  PubMed  CAS  Google Scholar 

  • Bennett MVL (1965) Electroreceptors in mormyrids. Cold Spring Harbor Symp Quant Biol 30:245–262.

    PubMed  CAS  Google Scholar 

  • Bennett MVL (1967) Mechanisms of electroreception. In Cahn P (ed), Lateral Line Detectors. Bloomington: Indiana University Press, pp. 313–393.

    Google Scholar 

  • Bennett MVL (1971) Electroreception. In Hoar WS, Randall DJ (eds), Fish Physiology, Vol. 5: Sensory Systems and Electric Organs. New York: Academic Press, pp. 493–574.

    Google Scholar 

  • Bennett MVL, Steinbach AB (1969) Influence of electric organ control system of electrosensory afferent pathways in mormyrids. In: Llinas R (ed), Neurobiology of Cerebellar Evolution and Development. Chicago: American Medical Association, pp. 207–214.

    Google Scholar 

  • Berman NJ, Maler L (1998a) Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus). J Neurophysiol 80:3173–3196.

    PubMed  CAS  Google Scholar 

  • Berman NJ, Maler L (1998b) Interaction of GABAB-mediated inhibition with voltagegated currents of pyramidal cells: computational mechanism of a sensory searchlight. J Neurophysiol 80:3197–3213.

    PubMed  CAS  Google Scholar 

  • Berman NJ, Maler L (1998c) Distal versus proximal inhibitory shaping of feedback excitation in the electrosensory lateral line lobe: implications for sensory filtering. J Neurophysiol 80:3214–3232.

    PubMed  CAS  Google Scholar 

  • Berman NJ, Maler L (1999) Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J Exp Biol 202:1243–1253.

    PubMed  Google Scholar 

  • Berman NJ, Hincke MT, Maler L (1995) Inositol 1,4,5-trisphosphate receptor localization in the brain of a weakly electric fish (Apteronotus leptorhynchus) with emphasis on the electrosensory system. J Comp Neurol 361:512–524.

    Article  PubMed  CAS  Google Scholar 

  • Berman NJ, Plant J, Turner RW, Maler L (1997) Excitatory amino acid receptors at a feedback pathway in the electrosensory system: implications for the searchlight hypothesis. J Neurophysiol 78:1869–1881.

    PubMed  CAS  Google Scholar 

  • Berman NJ, Dunn RJ, Maler L (2001) Function of NMDA receptors and persistent sodium channels in a feedback pathway of the electrosensory system. J Neurophysiol 86:1612–1621.

    PubMed  CAS  Google Scholar 

  • Bratton B, Bastian J (1990) Descending control of electroreception. II. Properties of nucleus praeeminentialis neurons projecting directly to the electrosensory lateral line lobe. J Neurosci 10:1241–1253.

    PubMed  CAS  Google Scholar 

  • Bullock TH, Chichibu S (1965) Further analysis of sensory coding in electroreceptors of electric fish. Proc Natl Acad Sci USA 54:422–429.

    Article  PubMed  CAS  Google Scholar 

  • Bullock TH, Hagiwara S, Kusano K, Negishi K (1961) Evidence for a category of electroreceptors in the lateral line of gymnotid fishes. Science 134:1426–1427.

    Google Scholar 

  • Bullock TH, Behrend K, Heiligenberg W (1975) Comparison of the jamming avoidance responses in Gymnotoid and Gymnarchid electric fish: a case of convergent evolution of behavior and its sensory basis. J Comp Physiol 103:97–121.

    Article  Google Scholar 

  • Carlson BA, Kawasaki M (2004) Nonlinear response properties of combination-sensitive electrosensory neurons in the midbrain of Gymnarchus niloticus. J Neurosci 24(37): 8039–8048.

    Article  PubMed  CAS  Google Scholar 

  • Carr C, Maler L (1986) Electroreception in gymnotiform fish. Central anatomy and physiology. Bullock TH, Heiligenberg W. (eds), Electroreception. New York: John Wiley & Sons

    Google Scholar 

  • Carr CE (1993) Processing of temporal information in the brain. Annu Rev Neurosci 16:223–243.

    Article  PubMed  CAS  Google Scholar 

  • Carr CE, Friedman MA (1999) Evolution of time coding systems. Neural Comput 11: 1–20.

    Article  PubMed  CAS  Google Scholar 

  • Carr CE, Maler L, Heiligenberg W, Sas E (1981) Laminar organization of the afferent and efferent systems of the torus semicircularis of Gymnotiform fish: morphological substrates for parallel processing in the electrosensory system. J Comp Neurol 203: 649–670.

    Article  PubMed  CAS  Google Scholar 

  • Carr CE, Maler L, Sas E (1982) Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol 211:139–153.

    Article  PubMed  CAS  Google Scholar 

  • Carr CE, Heiligenberg W, Rose GJ (1986a) A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 6:107–119.

    PubMed  CAS  Google Scholar 

  • Carr CE, Maler L, Taylor B (1986b) A time-comparison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 6:1372–1383.

    PubMed  CAS  Google Scholar 

  • Carr CE, Soares D, Parameshwaran S, Perney T (2001) Evolution and development of time coding systems. Curr Opin Neurobiol 11:727–733.

    Article  PubMed  CAS  Google Scholar 

  • Castello ME, Caputi A, Trujillo-Cenoz O (1998) Structural and functional aspects of the fast electrosensory pathway in the electrosensory lateral line lobe of the pulse fish Gymnotus carapo. J Comp Neurol 401:549–563.

    Article  PubMed  CAS  Google Scholar 

  • Chacron MJ, Doiron B, Maler L, Longtin A, Bastian J (2003) Non-classical receptive field mediates switch in a sensory neuron’s frequency tuning. Nature 423:77–81.

    Article  PubMed  CAS  Google Scholar 

  • Crawford AC, Fettiplace R (1981) An electrical tuning mechanism in turtle cochlear hair cells. J Physiol 312:377–422.

    PubMed  CAS  Google Scholar 

  • Crick F (1984) Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci USA 81:4586–4590.

    Article  PubMed  CAS  Google Scholar 

  • Doiron B, Longtin A, Berman N, Maler L (2001) Subtractive and divisive inhibition: effect of voltage-dependent inhibitory conductances and noise. Neural Comput 13: 227–248.

    Article  PubMed  CAS  Google Scholar 

  • Doiron B, Chacron MJ, Maler L, Longtin A, Bastian J (2003) Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli. Nature 421:539–543.

    Article  PubMed  CAS  Google Scholar 

  • Enger P, Szabo T (1965) Activity of central neurons involved in electroreception in some weakly electric fish (Gymnotidae). J Neurophysiol 28:800–818.

    PubMed  CAS  Google Scholar 

  • Fessard A, Szabo T (1961) Mise évidence d’un récepteur sensible à l’ électricité dans la peau d’un mormyre. C. rendu hebd. Séanc Acad Sci Paris 253:1859–1860.

    Google Scholar 

  • Fortune ES, Rose GJ (1996) Temporal filtering properties of midbrain neurons in an electric fish: implications for the function of dendritic spines. Neurosci Res 26:89–94.

    PubMed  Google Scholar 

  • Fortune ES, Rose GJ (1997a) Temporal filtering properties of ampullary electrosensory neurons in the torus semicircularis of Eigenmannia: evolutionary and computational implications. Brain Behav Evol 49:312–323.

    PubMed  CAS  Google Scholar 

  • Fortune ES, Rose GJ (1997b) Passive and active membrane properties contribute to the temporal filtering properties of midbrain neurons in vivo. J Neurosci 17:3815–3825.

    PubMed  CAS  Google Scholar 

  • Fortune ES, Rose GJ (2000) Short-term synaptic plasticity contributes to the temporal filtering of electrosensory information. J Neurosci 20:7122–7130.

    PubMed  CAS  Google Scholar 

  • Friedman MA, Hopkins CD (1998) Neural substrates for species recognition in the time-coding electrosensory pathway of mormyrid electric fish. J Neurosci 18:1171–1185.

    PubMed  CAS  Google Scholar 

  • Gabbiani F, Metzner W (1999) Encoding and processing of sensory information in neuronal spike trains. J Exp Biol 202:1267–1279.

    PubMed  Google Scholar 

  • Gabbiani F, Metzner W, Wessel R, Koch C (1996) From stimulus encoding to feature extraction in weakly electric fish. Nature 384:564–567.

    Article  PubMed  CAS  Google Scholar 

  • Gray CM, Konig P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334–337.

    Article  PubMed  CAS  Google Scholar 

  • Grothe B (2000) The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61:581–610.

    Article  PubMed  CAS  Google Scholar 

  • Grüsser OJ (1995) On the history of the ideas of efference copy and reafference. Clio Med 33:35–55.

    PubMed  Google Scholar 

  • Guo Y-X, Kawasaki M (1997) Representation of accurate temporal information in the electrosensory system of the African electric fish, Gymnarchus niloticus. J Neurosci 17:1761–1768.

    PubMed  CAS  Google Scholar 

  • Hagiwara S, Morita H (1963) Coding mechanisms of electroreceptor fibers in some electric fish. J Neurophysiol 26:551–567.

    PubMed  CAS  Google Scholar 

  • Hall C, Bell CC, Zelick R (1995) Behavioral evidence of a latency code for simulus intensity in mormyrid electric fish. J Comp Physiol 177:29–39.

    Article  Google Scholar 

  • Han VZ, Bell CC (2002) Cell morphology and local circuitry of the central lobes of the mormyrid cerebellum. Ann NY Acad Sci 978:515–516.

    Article  PubMed  Google Scholar 

  • Han VZ, Bell CC, Grant K, Sugawara Y (1999) Mormyrid electrosensory lobe in vitro: morphology of cells and circuits. J Comp Neurol 404:359–374.

    Article  PubMed  CAS  Google Scholar 

  • Harder W (1968) Die beziehungen zwischen elektrorezeptoren, elektrischem organ, seitenlinienorganen und nervensystem bei den Mormyridae (Teleostei, Pisces). Z Vergl Physiol 59:272–318.

    Google Scholar 

  • Heiligenberg W (1976) Electrolocation and jamming avoidance in the mormyrid fish Brienomyrus. J Comp Physiol 109:357–372.

    Article  Google Scholar 

  • Heiligenberg W (1977) Principles of Electrolocation and Jamming Avoidance in Electric Fish-A Neuroethological Approach. Berlin: Springer-Verlag.

    Google Scholar 

  • Heiligenberg W (1991a) Neural nets in electric fish. Cambridge, MA: MIT Press.

    Google Scholar 

  • Heiligenberg W (1991b) The neural basis of behavior: a neuroethological view. Annu Rev Neurosci 14:247–267.

    Article  PubMed  CAS  Google Scholar 

  • Heiligenberg W, Altes RA (1978) Phase sensitivity in electroreception. Science 199: 1001–1004.

    PubMed  CAS  Google Scholar 

  • Heiligenberg W, Bastian J (1980) The control of Eigenmannia’s pacemaker by distributed evaluation of electroreceptive afferences. J Comp Physiol 136:113–133.

    Article  Google Scholar 

  • Heiligenberg W, Dye J (1982) Labeling of electroreceptive afferents in gymnotid fish by intracellular injection of HRP: the mystery of multiple maps. J Comp Physiol 148:287–296.

    Article  Google Scholar 

  • Heiligenberg W, Baker C, Matsubara J (1978) The jamming avoidance response in Eigenmannia revisited: the structure of a neuronal democracy. J Comp Physiol 127:267–286.

    Article  Google Scholar 

  • Heiligenberg W, Rose GJ (1985) Phase and amplitude computations in the midbrain of an electric fish: intracellular studies of neurons participating in the jamming avoidance response of Eigenmannia. J Neurosci 5:515–531.

    PubMed  CAS  Google Scholar 

  • Heiligenberg W, Keller CH, Metzner W, Kawasaki M (1991) Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fish Eigenmannia: detection and processing of electric signals in social communication. J Comp Physiol 169:151–164.

    Article  CAS  Google Scholar 

  • Hopkins CD (1974) Electric communication in fish. Am Sci 62:426–437.

    PubMed  CAS  Google Scholar 

  • Hopkins CD (1976) Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J Comp Physiol 111:171–207.

    Article  Google Scholar 

  • Hopkins CD (1981) On the diversity of electric signals in a community of mormyrid electric fish in West Africa. Am Zool 21:211–222.

    Google Scholar 

  • Hopkins CD (1986a) Temporal structure of non-propagated electric communication signals. Brain Behav Evol 28:43–59.

    PubMed  CAS  Google Scholar 

  • Hopkins CD (1986b) Behavior of mormyridae. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 527–576.

    Google Scholar 

  • Hopkins CD (1995) Convergent designs for electrogenesis and electroreception. Curr Opin Neurobiol 5:769–777.

    Article  PubMed  CAS  Google Scholar 

  • Hopkins CD, Bass AH (1981) Temporal coding of species recognition signals in an electric fish. Science 212:85–87.

    PubMed  CAS  Google Scholar 

  • Irvine DR (1992) Physiology of auditory brainstem. In: Popper AN, Fay RR (eds), The Mammalian Auditory Pathway: Neurophysiology. New York: Springer-Verlag, pp. 153–231.

    Google Scholar 

  • Joris PX, Smith PH, Yin TC (1998) Coincidence detection in the auditory system: 50 years after Jeffress. Neuron 21:1235–1238.

    Article  PubMed  CAS  Google Scholar 

  • Kashimori Y, Inoue S, Kambara T (2001) A neural mechanism of hyperaccurate detection of phase advance and delay in the jamming avoidance response of weakly electric fish. Biol Cyber 85:117–131.

    Article  CAS  Google Scholar 

  • Kawasaki M (1993) Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnarchus niloticus. Comp Physiol A 173:9–22.

    CAS  Google Scholar 

  • Kawasaki M (1994) The African wave-type electric fish, Gymnarchus niloticus, lacks corollary discharge mechanisms for electrosensory gating. J Comp Physiol A 174: 133–144.

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki M (1996) Comparative analysis of the jamming avoidance response in African and South American wave-type fishes. Biol Bull 191:103–108.

    PubMed  CAS  Google Scholar 

  • Kawasaki M (1997) Sensory hyperacuity in the jamming avoidance response of weakly electric fish. Curr Opin Neurobiol 7:473–479.

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki M (2001) Cutaneous electrical oscillation in a weakly electric fish, Gymnarchus niloticus. J Comp Physiol A 187:597–604.

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki M, Guo Y-X (1996) Neuronal circuitry for comparison of timing in the electrosensory lateral line lobe of the African wave-type electric fish Gymnarchus niloticus. J Neurosci 16:380–391.

    PubMed  CAS  Google Scholar 

  • Kawasaki M, Guo Y-X (1998) Parallel projection of amplitude and phase information from the hindbrain to the midbrain of the African electric fish Gymnarchus niloticus. J Neurosci 18:7599–7611.

    PubMed  CAS  Google Scholar 

  • Kawasaki M, Guo Y-X (2002) Emergence of temporal-pattern sensitive neurons in the midbrain of weakly electric fish Gymnarchus niloticus. J Physiol Paris 96:531–537.

    Article  PubMed  Google Scholar 

  • Kawasaki M, Heiligenberg W (1988) Individual prepacemaker neurons can modulate the pacemaker cycle of the gymnotiform electric fish, Eigenmannia. J Comp Physiol 162: 13–21.

    Article  CAS  Google Scholar 

  • Kawasaki M, Maler L, Rose GJ, Heiligenberg W (1988a) Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus. J Comp Neurol 276:113–131.

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki M, Rose GJ, Heiligenberg W (1988b) Temporal hyperacuity in single neurons of electric fish. Nature 336:173–176.

    Article  PubMed  CAS  Google Scholar 

  • Keller CH (1988) Stimulus discrimination in the diencephalon of Eigenmannia: the emergence and sharpening of a sensory filter. J Comp Physiol 162:747–757.

    Article  CAS  Google Scholar 

  • Keller CH, Zakon HH, Sanchez DY (1986) Evidence for a direct effect of androgens upon electroreceptor tuning. J Comp Physiol 158:301–310.

    Article  CAS  Google Scholar 

  • Keller CH, Maler L, Heiligenberg W (1990) Structural and functional organization of a diencephalic sensory-motor interface in the gymnotiform fish, Eigenmannia. J Comp Neurol 293:347–376.

    Article  PubMed  CAS  Google Scholar 

  • Keller CH, Kawasaki M, Heiligenberg W (1991) The control of pacemaker modulations for social communication in the weakly electric fish Sternopygus. J Comp Physiol 169:441–450.

    Article  CAS  Google Scholar 

  • Koch C, Poggio T (1983) A theoretical analysis of electrical properties of spines. Proc R Soc Lond B Biol Sci 218:455–477.

    Article  PubMed  CAS  Google Scholar 

  • Laurent G (1996) Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci 19:489–496.

    Article  PubMed  CAS  Google Scholar 

  • Lemon N, Turner RW (2000) Conditional spike backpropagation generates burst discharge in a sensory neuron. J Neurophysiol 84:1519–1530.

    PubMed  CAS  Google Scholar 

  • Lissmann HW (1958) On the function and evolution of electric organs in fish. J Exp Biol 35:156–191.

    Google Scholar 

  • Lissmann HW, Machin KE (1958) The mechanism of object location in Gymnarchus niloticus and similar fish. J Exp Biol 35:451–486.

    Google Scholar 

  • Maler L, Sas E, Rogers J (1981) The cytology of the posterior lateral line lobe of high frequency weakly electric fish (Gymnotidae). Dendritic differentiation and synaptic specificity in a simple cortex. J Comp Neurol 195:87–139.

    Article  PubMed  CAS  Google Scholar 

  • Mathieson WB, Maler L (1988) Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice. J Comp Physiol 163:489–506.

    Article  CAS  Google Scholar 

  • Matsushita A, Kawasaki M (2004) Unitary giant synapses embracing a single neuron at the convergent site of time-coding pathways of an electric fish, Gymnarchus niloticus. J Comp Neurol 472(2):140–155.

    Article  PubMed  Google Scholar 

  • Meek J, Grant K, Bell CC (1999) Structural organization of the mormyrid electrosensory lateral line lobe. J Exp Biol 202:1291–1300.

    PubMed  Google Scholar 

  • Meek J, Hafmans TG, Han V, Bell CC, Grant K (2001) Myelinated dendrites in the mormyrid electrosensory lobe. J Comp Neurol 431:255–275.

    Article  PubMed  CAS  Google Scholar 

  • Metzner W (1993) The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways. J Neurosci 13:1862–1878.

    PubMed  CAS  Google Scholar 

  • Metzner W, Heiligenberg W (1991) The coding of signals in the electric communication of the gymnotiform fish Eigenmannia: from electroreceptors to neurons in the torus semicircularis of the midbrain. J Comp Physiol 169:135–150.

    Article  CAS  Google Scholar 

  • Metzner W, Juranek J (1997a) A sensory brain map for each behavior? Proc Natl Acad Sci USA 94(26):14798–14803.

    Article  PubMed  CAS  Google Scholar 

  • Metzner W, Juranek J (1997b) A method to biotinylate and histochemically visualize ibotenic acid for pharmacological inactivation studies. J Neurosci Methods 76(2):143–150.

    Article  PubMed  CAS  Google Scholar 

  • Metzner W, Koch C, Wessel R, Gabbiani F (1998) Feature extraction by burst-like spike patterns in multiple sensory maps. J Neurosci 18:2283–2300.

    PubMed  CAS  Google Scholar 

  • Meyer J (1982) Behavioral response of weakly electric fish to complex impedances. J Comp Physiol 145:459–470.

    Article  Google Scholar 

  • Meyer JH, Bell CC (1983) Sensory gating by a corollary discharge mechanism. J Comp Physiol 151:401–406.

    Article  Google Scholar 

  • Mohr C, Roberts PD, Bell CC (2003a) Cells of the mormyromast region of the mormyrid electrosensory lobe: I. Responses to the electric organ corollary disharge and to electrosensory stimuli. J Neurophysiol 90:1193–1210.

    Article  PubMed  Google Scholar 

  • Mohr C, Roberts PD, Bell CC (2003b) Cells of the mormyromast region of the mormyrid electrosensory lobe: II. Responsese to input from central sources. J Neurophysiol 90: 1211–1223.

    Article  PubMed  Google Scholar 

  • Mugnaini E, Maler L (1987a) Cytology and immunocytochemistry of the nucleus exterolateralis anterior of the mormyrid brain: possible role of GABAergic synapses in temporal analysis. Anat Embryol (Berl) 176:313–336.

    Article  PubMed  CAS  Google Scholar 

  • Mugnaini E, Maler L (1987b) Cytology and immunocytochemistry of the nucleus of the lateral line lobe in the electric fish Gnathonemus petersii (Mormyridae): evidence suggesting that GABAergic synapses mediate an inhibitory corollary discharge. Synapse 1:32–56.

    Article  PubMed  CAS  Google Scholar 

  • Murthy VN, Fetz EE (1996) Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J Neurophysiol 76:3968–3982.

    PubMed  CAS  Google Scholar 

  • Naruse M, Kawasaki M (1998) Possible involvement of the ampullary electroreceptor system in detection of frequency-modulated electrocommunication signals in Eigenmannia. J Comp Physiol 183:543–552.

    Article  CAS  Google Scholar 

  • Poor H (1994) An introduction to signal detection and estimation. New York: Springer-Verlag.

    Google Scholar 

  • Ramanathan K, Michael TH, Jiang GJ, Hiel H, Fuchs PA (1999) A molecular mechanism for electrical tuning of cochlear hair cells. Science 283:215–217.

    Article  PubMed  CAS  Google Scholar 

  • Réthelyi M, Szabo T (1973) A particular nucleus in the mesencephalon of weakly electric fish, Gymnotus carapo (Gymnotidae, Pisces). Exp Brain Res 17:229–241.

    Article  PubMed  Google Scholar 

  • Rose GJ, Call SJ (1992) Evidence for the role of dendritic spines in the temporal filtering properties of neurons: the decoding problem and beyond. Proc Natl Acad Sci USA 89:9662–9665.

    Article  PubMed  CAS  Google Scholar 

  • Rose GJ, Call SJ (1993) Temporal filtering properties of midbrain neurons in an electric fish: implications for the function of dendritic spines. J Neurosci 13:1178–1189.

    PubMed  CAS  Google Scholar 

  • Rose GJ, Fortune ES (1996) New techniques for making whole-cell recordings from CNS neurons in vivo. Neurosci Res 26:89–94.

    PubMed  CAS  Google Scholar 

  • Rose GJ, Fortune ES (1999) Frequency-dependent PSP depression contributes to low-pass temporal filtering in Eigenmannia. J Neurosci 19:7629–7639.

    PubMed  CAS  Google Scholar 

  • Rose GJ, Heiligenberg W (1985a) Structure and function of electrosensory neurons in the torus semicircularis of Eigenmannia: morphological correlates of phase and amplitude sensitivity. J Neurosci 5:2269–2280.

    PubMed  CAS  Google Scholar 

  • Rose GJ, Heiligenberg W (1985b) Temporal hyperacuity in the electric sense of fish. Nature 318:178–180.

    Article  PubMed  CAS  Google Scholar 

  • Rose GJ, Heiligenberg W (1986a) Neural coding of difference frequencies in the midbrain of the electric fish Eigenmannia: reading the sense of rotation in an amplitude-phase plane. J Comp Physiol 158:613–624.

    Article  CAS  Google Scholar 

  • Rose GJ, Heiligenberg W (1986b) Limits of phase and amplitude sensitivity in the torus semicircularis of Eigenmannia. J Comp Physiol 159:813–822.

    Article  CAS  Google Scholar 

  • Rose GJ, Keller CH, Heiligenberg W (1987) “Ancestral” neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response. J Comp Physiol 160:491–500.

    Article  CAS  Google Scholar 

  • Rose GJ, Kawasaki M, Heiligenberg W (1988) “Recognition units” at the top of a euronal hierarchy? Prepacemaker neurons in Eigenmannia code the sign of frequency differences unambiguously. J Comp Physiol 162:759–772.

    Article  CAS  Google Scholar 

  • Russell CJ, Bell CC (1978) Neuronal responses to electrosensory input in mormyrid valvula cerebelli. J Neurophysiol 41:1495–1510.

    PubMed  CAS  Google Scholar 

  • Sas E, Maler L (1983) The nucleus praeeminentials: a Golgi study of a feedback center in the electrosensory system of gymnotiform fish. J Comp Neurol 221:127–144.

    Article  PubMed  CAS  Google Scholar 

  • Saunders J, Bastian J (1984) The physiology and morphology of two types of electrosensory neurons in the weakly electric fish Apteronotus leptorhynchus. J Comp Physiol 154:199–209.

    Article  Google Scholar 

  • Scheich H, Bullock TH (1974) The detection of electric fields from electric organs. In: Fessard A (ed), Handbook of Sensory Physiology, Vol. III/3: Electroreceptors and Other Specialized Receptors in Lower Vertebrates, Berlin: Springer-Verlag, pp. 201–256.

    Google Scholar 

  • Scheich H, Bullock TH, Hamstra RH (1973) Coding properties of two classes of afferent nerve fibers: high-frequency electroreceptors in the electric fish, Eigenmannia. J Neurophysiol 36:39–60.

    PubMed  CAS  Google Scholar 

  • Shuai J, Kashimori Y, Kambara T (1998) Electroreceptor model of the weakly electric fish Gnathonemus petersii. I. The model and the origin of differences between A-and B-receptors. Biophys J 75:1712–1726.

    PubMed  CAS  Google Scholar 

  • Shuai J, Kashimori Y, Hoshino O, Kambara T, von der Emde G (1999) Electroreceptor model of weakly electric fish Gnathonemus petersii: II. Cellular origin of inverse waveform tuning. Biophys J 76:3012–3025.

    Article  PubMed  CAS  Google Scholar 

  • Shumway CA (1989a) Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I. Physiological differences. J Neurosci 9:4388–4399.

    PubMed  CAS  Google Scholar 

  • Shumway CA (1989b) Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences. J Neurosci 9:4400–4415.

    PubMed  CAS  Google Scholar 

  • Shumway CA, Maler L (1989) GABAergic inhibition shapes temporal and spatial response properties of pyramidal cells in the electrosensory lateral line lobe of gymnotiform fish. J Comp Physiol 164:391–407.

    Article  CAS  Google Scholar 

  • Simmons JA, Saillant PA, Ferragamo MJ, Haresign T, Dear SP, Fritz J, McMullen TA (1995) Auditory computations for biosonar target imaging in bats. In: Hawkins HL, McMullen TA, Popper AN, Fay RR (eds), Auditory Computation. NewYork: Springer-Verlag, pp. 401–468.

    Google Scholar 

  • Smotherman MS, Narins PM (1999) The electrical properties of auditory hair cells in the frog amphibian papilla. J Neurosci 19:5275–5292.

    PubMed  CAS  Google Scholar 

  • Sperry R (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Phyiol Psychol 43:482–489.

    Article  CAS  Google Scholar 

  • Sugawara Y, Grant K, Han V, Bell CC (1999) Physiology of electrosensory lateral line lobe neurons in Gnathonemus petersii. J Exp Biol 202:1301–1309.

    PubMed  CAS  Google Scholar 

  • Szabo T (1965) Sense organs of the lateral line system in some electric fish of the Gymnotidae, Mormyridae and Gymnarchidae. J Morphol 117:229–250.

    Article  PubMed  CAS  Google Scholar 

  • Szabo T (1967) Activity of peripheral and central neurones involved in electroreception In: Cahn PH (ed), Lateral Line Detectors. Bloomington, IN: Indiana University Press, pp. 295–311.

    Google Scholar 

  • Szabo T (1974) Anatomy of the specialized lateral line organs of electroreception, In: Fessard A (ed), Handbook of Sensory Physiology, Vol. III/3: Electroreceptors and Other Specialized Receptors in Lower Vertebrates. Berlin: Springer-Verlag, pp. 13–58.

    Google Scholar 

  • Szabo T, Fessard A (1974) Physiology of electroreceptors. In: Fessard A (ed), Handbook of Sensory Physiology, Vol. III/3: Electroreceptors and Other Specialized Receptors in Lower Vertebrates. Berlin: Springer-Verlag, pp. 59–124.

    Google Scholar 

  • Szabo T, Hagiwara S (1967) A latency change mechanisms involved in sensory coding of electric fish (mormyrids). Physiol Behav 2:331–335.

    Article  Google Scholar 

  • Takagi H, Kawasaki M (2003) Modeling of time disparity detection by the Hodgkin-Huxley equations. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189: 257–262.

    PubMed  CAS  Google Scholar 

  • Takizawa Y, Rose GJ, Kawasaki M (1999) Resolving competing theories for control of the jamming avoidance response: the role of amplitude modulations in electric organ discharge decelerations. J Exp Biol 202:1377–1386.

    PubMed  CAS  Google Scholar 

  • Trussell LO (1999) Synaptic mechanisms for coding timing in auditory neurons. Annu Rev Physiol 61:477–496.

    Article  PubMed  CAS  Google Scholar 

  • Turner RW, Maler L, Deerinck T, Levinson SR, Ellisman MH (1994) TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron. J Neurosci 14:6453–6471.

    PubMed  CAS  Google Scholar 

  • Turner RW, Plant JR, Maler L (1996) Oscillatory and burst discharge across electrosensory topographic maps. J Neurophysiol 76:2364–2382.

    PubMed  CAS  Google Scholar 

  • von der Emde G (1992) Electrolocation of capacitive objects in four species of pulsetype weakly electric fish. II. Electric signalling behaviour. Ethology 92:177–192.

    Article  Google Scholar 

  • von der Emde G (1993) Capacitance discrimination in electrolocating weakly electric pulse-fish. Naturwiss 80:231–233.

    Article  Google Scholar 

  • von der Emde G (1997) Electroreception. In: Evans D (ed), The Physiology of Fishes Boca Raton: CRC Press, pp. 313–343.

    Google Scholar 

  • von der Emde G (1998) Capacitance detection in the wave-type electric fish Eigenmannia during active electrolocation. J Comp Physiol 182:217–224.

    Article  Google Scholar 

  • von der Emde G, Bell CC (1994) Responses of cells in the mormyrid electrosensory lobe to EODs with distorted wave-forms: implications for capacitance detection. J Comp Physiol 175:83–93.

    Google Scholar 

  • von der Emde G, Bell CC (1996) The nucleus preeminentialis of mormyrid fish, a center for recurrent electrosensory feedback: I. Electrosensory and corollary discharge responses. J Neurophysiol 76:1581–1596.

    PubMed  Google Scholar 

  • von der Emde G, Bleckmann H (1997) Waveform tuning of electroreceptor cells in the weakly electric fish, Gnathonemus petersii. J Comp Physiol 181:511–524.

    Article  Google Scholar 

  • von der Emde G, Ringer T (1992) Electrolocation of capacitive objects in four species of pulse-type weakly electric fish. I. Discrimination performance. Ethology 91:326–338.

    Google Scholar 

  • von Holst E, Mittelstaedt H (1950) Das Reafferenz-Prinzip. Naturwiss 37:464–476.

    Article  Google Scholar 

  • Wessel W, Koch C, Gabbiani F (1996) Coding of time-varying electric field amplitude modulations in a wave-type electric fish. J Neurophysiol 75:2280–2293.

    PubMed  CAS  Google Scholar 

  • Wu YC, Art JJ, Goodman MB, Fettiplace R (1995) A kinetic description of the calcium-activated potassium channel and its application to electrical tuning of hair cells. Prog Biophys Mol Biol 63:131–158.

    Article  PubMed  CAS  Google Scholar 

  • Zakon H (1986) The electroreceptive periphery. In: Bullock TH (ed), Electroreception. New York: John Wiley & Sons, pp. 103–156.

    Google Scholar 

  • Zakon HH, Meyer JH (1983) Plasticity of electroreceptor tuning in the weakly electric fish, Sternopygus dariensis. J Comp Physiol 153:477–487.

    Article  Google Scholar 

  • Zakon HH, Yan HY, Thomas P (1990) Human chorionic gonadotropin-induced shifts in the electrosensory system of the weakly electric fish, Sternopygus. J Neurobiol 21: 826–833.

    Article  PubMed  CAS  Google Scholar 

  • Zipser B, Bennett MVL (1976a) Responses of cells of the posterior lateral line lobe to activation of electroreceptors in a mormyrid fish. J Neurophysiol 39:693–712.

    PubMed  CAS  Google Scholar 

  • Zipser B, Bennett MVL (1976b) Interaction of electrosensory and electromotor signals in lateral line lobe of a mormyrid fish. J Neurophysiol 39:713–721.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Virginia, Charlottesville, VA, 22904, USA

    Masashi Kawasaki

Authors
  1. Masashi Kawasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Neurosciences School of Medicine, University of California, San Diego, La Jolla, CA, 92093-0240, USA

    Theodore H. Bullock

  2. Department of Neurobiology & Behavior, Cornell University, Ithaca, NY, 14583, USA

    Carl D. Hopkins

  3. Department of Biology, University of Maryland, College Park, MD, 20742, USA

    Arthur N. Popper

  4. Parmly Hearing Institute and Department of Psychology, Loyola University of Chicago, Chicago, IL, 60626, USA

    Richard R. Fay

Rights and permissions

Reprints and permissions

Copyright information

© 2005 Springer Science+Business Media, Inc.

About this chapter

Cite this chapter

Kawasaki, M. (2005). Physiology of Tuberous Electrosensory Systems. In: Bullock, T.H., Hopkins, C.D., Popper, A.N., Fay, R.R. (eds) Electroreception. Springer Handbook of Auditory Research, vol 21. Springer, New York, NY . https://doi.org/10.1007/0-387-28275-0_7

Download citation

Publish with us

Policies and ethics

Search

Navigation