Physiology of Tuberous Electrosensory Systems

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.

[1]  V. Han,et al.  Mormyrid electrosensory lobe in vitro: Morphology of cells and circuits , 1999, The Journal of comparative neurology.

[2]  L. Maler,et al.  Distal versus proximal inhibitory shaping of feedback excitation in the electrosensory lateral line lobe: implications for sensory filtering. , 1998, Journal of neurophysiology.

[3]  Maurice J Chacron,et al.  Receptive Field Organization Determines Pyramidal Cell Stimulus-Encoding Capability and Spatial Stimulus Selectivity , 2002, The Journal of Neuroscience.

[4]  L. Maler,et al.  Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus). , 1998, Journal of neurophysiology.

[5]  T Szabo,et al.  Pathways of the electric organ discharge command and its corollary discharges in mormyrid fish , 1983, The Journal of comparative neurology.

[6]  W Heiligenberg,et al.  Phase and amplitude computations in the midbrain of an electric fish: intracellular studies of neurons participating in the jamming avoidance response of Eigenmannia , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  P. Fuchs,et al.  A molecular mechanism for electrical tuning of cochlear hair cells. , 1999, Science.

[8]  M. Réthelyi,et al.  A particular nucleus in the mesencephalon of a weakly electric fish, gymnotus carapo, gymnotidae , 1973, Experimental Brain Research.

[9]  James A. Simmons,et al.  Auditory Computations for Biosonar Target Imaging in Bats , 1996 .

[10]  Emergence of temporal-pattern sensitive neurons in the midbrain of weakly electric fish Gymnarchus niloticus , 2002, Journal of Physiology-Paris.

[11]  C. Carr,et al.  Evolution and development of time coding systems , 2001, Current Opinion in Neurobiology.

[12]  Leonard Maler,et al.  GABAergic inhibition shapes temporal and spatial response properties of pyramidal cells in the electrosensory lateral line lobe of gymnotiform fish , 2004, Journal of Comparative Physiology A.

[13]  F Gabbiani,et al.  Feature Extraction by Burst-Like Spike Patterns in Multiple Sensory Maps , 1998, The Journal of Neuroscience.

[14]  J. Juranek,et al.  A sensory brain map for each behavior? , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[15]  G. von der Emde,et al.  Electric organ corollary discharge pathways in mormyrid fish , 1995, Journal of Comparative Physiology A.

[16]  W. Heiligenberg.  The neural basis of behavior: a neuroethological view. , 1991, Annual review of neuroscience.

[17]  Susumu Hagiwara,et al.  A latency-change mechanism involved in sensory coding of electric fish (mormyrids) , 1967 .

[18]  L. Maler,et al.  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 , 1987, Synapse.

[19]  G. von der Emde,et al.  Waveform tuning of electroreceptor cells in the weakly electric fish, Gnathonemus petersii , 1997, Journal of Comparative Physiology A.

[20]  Stimulus discrimination in the diencephalon ofEigenmannia: the emergence and sharpening of a sensory filter , 1988, Journal of Comparative Physiology A.

[21]  C. Bell,et al.  Central connections of the posterior lateral line lobe in mormyrid fish , 2004, Experimental Brain Research.

[22]  M. Kawasaki,et al.  Modeling of time disparity detection by the Hodgkin-Huxley equations , 2003, Journal of Comparative Physiology A.

[23]  L. Maler,et al.  Inositol 1,4,5‐trisphosphate receptor localization in the brain of a weakly electric fish (Apteronotus leptorhynchus) with emphasis on the electrosensory system , 1995, The Journal of comparative neurology.

[24]  F. Crick.  Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[25]  John Tyler Bonner,et al.  Evolution and Development , 1998 .

[26]  Joseph Bastian,et al.  The physiology and morphology of two types of electrosensory neurons in the weakly electric fishApteronotus leptorhynchus , 1984, Journal of Comparative Physiology A.

[27]  A H Bass,et al.  Temporal coding of species recognition signals in an electric fish. , 1981, Science.

[28]  L. Maler,et al.  Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering , 1999, The Journal of experimental biology.

[29]  Walter Heiligenberg,et al.  Temporal hyperacuity in the electric sense of fish , 1985, Nature.

[30]  A. Bass,et al.  Comparative aspects of brain organization of an african “wave” electric fish, Gymnarchus niloticus , 1982, Journal of morphology.

[31]  L. Trussell,et al.  Synaptic mechanisms for coding timing in auditory neurons. , 1999, Annual review of physiology.

[32]  W. Heiligenberg,et al.  Phase sensitivity in electroreception. , 1978, Science.

[33]  K. E. Machin,et al.  The Mechanism of Object Location in Gymnarchus Niloticus and Similar Fish , 1958 .

[34]  M. Réthelyi,et al.  Neurohistological analysis of the lateral lobe in a weakly electric fish, Gymnotus carapo (Gymnotidae, Pisces) , 1973, Experimental Brain Research.

[35]  Walter Heiligenberg,et al.  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 , 1991, Journal of Comparative Physiology A.

[36]  L. Maler,et al.  The cytology of the posterior lateral line lobe of high‐frequency weakly electric fish (gymnotidae): Dendritic differentiation and synaptic specificity in a simple cortex , 1981, The Journal of comparative neurology.

[37]  C. Carr,et al.  A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  R. Fettiplace,et al.  An electrical tuning mechanism in turtle cochlear hair cells , 1981, The Journal of physiology.

[39]  Joseph Bastian,et al.  Frequency response characteristics of electroreceptors in weakly electric fish (Gymnotoidei) with a pulse discharge , 1976, Journal of comparative physiology.

[40]  Physiology of electrosensory lateral line lobe neurons in Gnathonemus petersii. , 1999, The Journal of experimental biology.

[41]  Gary J. Rose,et al.  Frequency-Dependent PSP Depression Contributes to Low-Pass Temporal Filtering in Eigenmannia , 1999, The Journal of Neuroscience.

[42]  G. von der Emde,et al.  Capacitance detection in the wave-type electric fish Eigenmannia during active electrolocation , 1998, Journal of Comparative Physiology A.

[43]  Philip H Smith,et al.  Coincidence Detection in the Auditory System 50 Years after Jeffress , 1998, Neuron.

[44]  K. Grant,et al.  Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  Masashi Kawasaki,et al.  Unitary giant synapses embracing a single neuron at the convergent site of time‐coding pathways of an electric fish, Gymnarchus niloticus , 2004, The Journal of comparative neurology.

[46]  Brent Doiron,et al.  Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli , 2003, Nature.

[47]  G. Laurent.  Dynamical representation of odors by oscillating and evolving neural assemblies , 1996, Trends in Neurosciences.

[48]  Wilhelm Harder,et al.  Die Beziehungen zwischen Elektrorezeptoren, Elektrischem Organ, Seitenlinienorganen und Nervensystem bei den Mormyridae (Teleostei, Pisces) , 1968, Zeitschrift für vergleichende Physiologie.

[49]  M. Kawasaki.  Cutaneous electrical oscillation in a weakly electric fish, Gymnarchus niloticus , 2001, Journal of Comparative Physiology A.

[50]  M. Kawasaki,et al.  Possible involvement of the ampullary electroreceptor system in detection of frequency-modulated electrocommunication signals in Eigenmannia , 1998, Journal of Comparative Physiology A.

[51]  Brent Doiron,et al.  Subtractive and Divisive Inhibition: Effect of Voltage-Dependent Inhibitory Conductances and Noise , 2001, Neural Computation.

[52]  Walter Heiligenberg,et al.  The coding of signals in the electric communication of the gymnotiform fish Eigenmannia: From electroreceptors to neurons in the torus semicircularis of the midbrain , 1991, Journal of Comparative Physiology A.

[53]  C. Bell,et al.  Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. III. Physiological differences between two morphological types of fibers. , 1990, Journal of neurophysiology.

[54]  Walter Heiligenberg,et al.  Electrolocation and jamming avoidance in the mormyrid fishBrienomyrus , 2004, Journal of comparative physiology.

[55]  A. Caputi,et al.  Structural and functional aspects of the fast electrosensory pathway in the electrosensory lateral line lobe of the pulse fish Gymnotus carapo , 1998, The Journal of comparative neurology.

[56]  M. Kawasaki,et al.  ‘Recognition units’ at the top of a neuronal hierarchy? , 2004, Journal of Comparative Physiology A.

[57]  Brent Doiron,et al.  Non-classical receptive field mediates switch in a sensory neuron's frequency tuning , 2003, Nature.

[58]  S. Hagiwara,et al.  Coding mechanisms of electro-receptor fibers in some electric fish. , 1963, Journal of neurophysiology.

[59]  Curtis C Bell,et al.  The mormyromast region of the mormyrid electrosensory lobe. II. Responses to input from central sources. , 2003, Journal of neurophysiology.

[60]  C. Bell,et al.  Electric organ corollary discharge pathways in mormyrid fish , 1995, Journal of Comparative Physiology A.

[61]  E. Fortune,et al.  Passive and Active Membrane Properties Contribute to the Temporal Filtering Properties of Midbrain Neurons In Vivo , 1997, The Journal of Neuroscience.

[62]  J. Juranek,et al.  A method to biotinylate and histochemically visualize ibotenic acid for pharmacological inactivation studies , 1997, Journal of Neuroscience Methods.

[63]  J. Bastian.  Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  C E Carr,et al.  Laminar organization of the afferent and efferent systems of the torus semicircularis of Gymnotiform fish: Morphological substrates for parallel processing in the electrosensory system , 1981, The Journal of comparative neurology.

[65]  C. Bell,et al.  Behavioral evidence of a latency code for stimulus intensity in mormyrid electric fish , 1995, Journal of Comparative Physiology A.

[66]  C. Hopkins,et al.  Temporal structure of non-propagated electric communication signals. , 1986, Brain, behavior and evolution.

[67]  C A Shumway,et al.  Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  W. Heiligenberg,et al.  Neural correlates of the jamming avoidance response ofEigenmannia , 1980, Journal of comparative physiology.

[69]  M. Kawasaki,et al.  Parallel Projection of Amplitude and Phase Information from the Hindbrain to the Midbrain of the African Electric Fish Gymnarchus niloticus , 1998, The Journal of Neuroscience.

[70]  Walter Heiligenberg,et al.  Neural Nets in Electric Fish , 1991 .

[71]  J. Bastian,et al.  Plasticity in an electrosensory system. III. Contrasting properties of spatially segregated dendritic inputs. , 1998, Journal of neurophysiology.

[72]  Yoshiki Kashimori,et al.  A neural mechanism of hyperaccurate detection of phase advance and delay in the jamming avoidance response of weakly electric fish , 2001, Biological Cybernetics.

[73]  P. Narins,et al.  The Electrical Properties of Auditory Hair Cells in the Frog Amphibian Papilla , 1999, The Journal of Neuroscience.

[74]  M. A. Friedman,et al.  Neural Substrates for Species Recognition in the Time-Coding Electrosensory Pathway of Mormyrid Electric Fish , 1998, The Journal of Neuroscience.

[75]  B. Zipser,et al.  Responses of cells of posterior lateral line lobe to activation of electroreceptors in a mormyrid fish. , 1976, Journal of neurophysiology.

[76]  Carl D. Hopkins,et al.  Stimulus filtering and electroreception: Tuberous electroreceptors in three species of Gymnotoid fish , 2004, Journal of comparative physiology.

[77]  T Kambara,et al.  Electroreceptor model of weakly electric fish Gnathonemus petersii: II. Cellular origin of inverse waveform tuning. , 1999, Biophysical journal.

[78]  O. Grüsser,et al.  On the history of the ideas of efference copy and reafference. , 1995, Clio medica.

[79]  D. Irvine.  Physiology of the Auditory Brainstem , 1992 .

[80]  Catherine E. Carr,et al.  Evolution of Time Coding Systems , 1999, Neural Computation.

[81]  The control of pacemaker modulations for social communication in the weakly electric fish Sternopygus , 1991, Journal of Comparative Physiology A.

[82]  Walter Heiligenberg,et al.  The control ofEigenmannia's pacemaker by distributed evaluation of electroreceptive afferences , 1980, Journal of comparative physiology.

[83]  Walter Heiligenberg,et al.  Principles of Electrolocation and Jamming Avoidance in Electric Fish , 1977, Studies of Brain Function.

[84]  Harold H. Zakon,et al.  Evidence for a direct effect of androgens upon electroreceptor tuning , 1986, Journal of Comparative Physiology A.

[85]  Walter Heiligenberg,et al.  Limits of phase and amplitude sensitivity in the torus semicircularis ofEigenmannia , 1986, Journal of Comparative Physiology A.

[86]  G. Rose,et al.  Neural coding of difference frequencies in the midbrain of the electric fishEigenmannia: Reading the sense of rotation in an amplitude-phase plane , 1986, Journal of Comparative Physiology A.

[87]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[88]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[89]  C. Carr,et al.  Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish , 1982, The Journal of comparative neurology.

[90]  M Kawasaki,et al.  Comparative analysis of the jamming avoidance response in African and South American wave-type electric fishes. , 1996, The Biological bulletin.

[91]  K. Grant,et al.  Sensory processing and corollary discharge effects in the mormyromast regions of the mormyrid electrosensory lobe. I. Field potentials, cellular activity in associated structures. , 1992, Journal of neurophysiology.

[92]  C. C. Bell,et al.  Effect of electric organ discharge on ampullary receptors in a mormyrid , 1978, Brain Research.

[93]  T Kambara,et al.  Electroreceptor model of the weakly electric fish Gnathonemus petersii. I. The model and the origin of differences between A- and B-receptors. , 1998, Biophysical journal.

[94]  Theodore H. Bullock,et al.  Evidence for a Category of Electroreceptors in the Lateral Line of Gymnotid Fishes , 1993 .

[95]  Leonard Maler,et al.  Cytology and immunocytochemistry of the nucleus extrolateralis anterior of the mormyrid brain: possible role of GABAergic synapses in temporal analysis , 2004, Anatomy and Embryology.

[96]  L. Maler,et al.  Oscillatory and burst discharge across electrosensory topographic maps. , 1996, Journal of neurophysiology.

[97]  Leonard Maler,et al.  Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice , 1988, Journal of Comparative Physiology A.

[98]  Walter Heiligenberg,et al.  Temporal hyperacuity in single neurons of electric fish , 1988, Nature.

[99]  S. Amagai,et al.  Time coding in the midbrain of mormyrid electric fish. II. Stimulus selectivity in the nucleus exterolateralis pars posterior , 1998, Journal of Comparative Physiology A.

[100]  C. Koch,et al.  Coding of time-varying electric field amplitude modulations in a wave-type electric fish. , 1996, Journal of neurophysiology.

[101]  G. von der Emde,et al.  Responses of cells in the mormyrid electrosensory lobe to EODs with distorted waveforms: implications for capacitance detection , 1994, Journal of Comparative Physiology A.

[102]  Sensory gating by a corollary discharge mechanism , 1983, Journal of comparative physiology.

[103]  G. Rose,et al.  Structure and function of electrosensory neurons in the torus semicircularis of Eigenmannia: morphological correlates of phase and amplitude sensitivity , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[104]  T Szabo,et al.  Activity of central neurons involved in electroreception in some weakly electric fish (Gymnotidae). , 1965, Journal of neurophysiology.

[105]  M. Kawasaki,et al.  Representation of Accurate Temporal Information in the Electrosensory System of the African Electric Fish,Gymnarchus niloticus , 1997, The Journal of Neuroscience.

[106]  C H Keller,et al.  Structural and functional organization of a diencephalic sensory‐motor interface in the gymnotiform fish, Eigenmannia , 1990, The Journal of comparative neurology.

[107]  V. Han,et al.  Myelinated dendrites in the mormyrid electrosensory lobe , 2001, The Journal of comparative neurology.

[108]  C C Bell,et al.  Nucleus preeminentialis of mormyrid fish, a center for recurrent electrosensory feedback. I. Electrosensory and corollary discharge responses. , 1996, Journal of neurophysiology.

[109]  M. Kawasaki,et al.  Nonlinear Response Properties of Combination-Sensitive Electrosensory Neurons in the Midbrain of Gymnarchus niloticus , 2004, The Journal of Neuroscience.

[110]  Meek,et al.  Structural organization of the mormyrid electrosensory lateral line lobe , 1999, The Journal of experimental biology.

[111]  R. Sperry.  Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[112]  J. Bastian.  Variations in the frequency response of electroreceptors dependent on receptor location in weakly electric fish (Gymnotoidei) with a pulse discharge , 2004, Journal of comparative physiology.

[113]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[114]  R. H. Hamstra,et al.  Coding properties of two classes of afferent nerve fibers: high-frequency electroreceptors in the electric fish, Eigenmannia. , 1973, Journal of neurophysiology.

[115]  C. Koch,et al.  From stimulus encoding to feature extraction in weakly electric fish , 1996, Nature.

[116]  Carl D Hopkins,et al.  Convergent designs for electrogenesis and electroreception , 1995, Current Opinion in Neurobiology.

[117]  B. Zipser,et al.  Interaction of electrosensory and electromotor signals in lateral line lobe of a mormyrid fish. , 1976, Journal of neurophysiology.

[118]  Walter Heiligenberg,et al.  The Jamming Avoidance Response inEigenmannia revisited: The structure of a neuronal democracy , 1978, Journal of comparative physiology.

[119]  Joseph Bastian,et al.  Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[120]  G. von der Emde,et al.  Capacitance discrimination in electrolocating, weakly electric pulse fish , 1993, Naturwissenschaften.

[121]  T H Bullock,et al.  Further analysis of sensory coding in electroreceptors of electric fish. , 1965, Proceedings of the National Academy of Sciences of the United States of America.

[122]  H. Vincent Poor,et al.  An Introduction to Signal Detection and Estimation , 1994, Springer Texts in Electrical Engineering.

[123]  G. Rose,et al.  Resolving competing theories for control of the jamming avoidance response: the role of amplitude modulations in electric organ discharge decelerations. , 1999, The Journal of experimental biology.

[124]  J Bastian.  Plasticity in an electrosensory system. II. Postsynaptic events associated with a dynamic sensory filter. , 1996, Journal of neurophysiology.

[125]  E. Fortune,et al.  Short-Term Synaptic Plasticity Contributes to the Temporal Filtering of Electrosensory Information , 2000, The Journal of Neuroscience.

[126]  T. Bullock,et al.  Comparison of the jamming avoidance responses in Gymnotoid and Gymnarchid electric fish: A case of convergent evolution of behavior and its sensory basis , 1975, Journal of comparative physiology.

[127]  G. Rose,et al.  Evidence for the role of dendritic spines in the temporal filtering properties of neurons: the decoding problem and beyond. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[128]  M. Kawasaki,et al.  Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnarchus niloticus , 1993, Journal of Comparative Physiology A.

[129]  G. Rose,et al.  Temporal filtering properties of midbrain neurons in an electric fish: implications for the function of dendritic spines , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[130]  H. W. Lissmann.  On the Function and Evolution of Electric Organs in Fish , 1958 .

[131]  L Maler,et al.  The nucleus praeeminentialis: A Golgi study of a feedback center in the electrosensory system of gymnotid fish , 1983, The Journal of comparative neurology.

[132]  Masashi Kawasaki,et al.  Sensory hyperacuity in the jamming avoidance response of weakly electric fish , 1997, Current Opinion in Neurobiology.

[133]  Catherine E. Carr,et al.  Processing of Temporal Information in the Brain , 1993 .

[134]  M. Kawasaki,et al.  The African wave-type electric fish, Gymnarchus niloticus, lacks corollary discharge mechanisms for electrosensory gating , 1994, Journal of Comparative Physiology A.

[135]  R. Fettiplace,et al.  A kinetic description of the calcium-activated potassium channel and its application to electrical tuning of hair cells. , 1995, Progress in biophysics and molecular biology.

[136]  T Szabo,et al.  Sense organs of the lateral line system in some electric fish of the Gymnotidae, Mormyridae and Gymnarchidae , 1965, Journal of morphology.

[137]  Curtis C Bell,et al.  The mormyromast region of the mormyrid electrosensory lobe. I. Responses to corollary discharge and electrosensory stimuli. , 2003, Journal of neurophysiology.

[138]  W Heiligenberg,et al.  Phase-sensitive midbrain neurons in Eigenmannia: neural correlates of the jamming avoidance response. , 1980, Science.

[139]  T. Poggio,et al.  A theoretical analysis of electrical properties of spines , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[140]  A. Bass,et al.  Shifts in frequency tuning of electroreceptors in androgen-treated mormyrid fish , 1984, Journal of Comparative Physiology A.

[141]  ‘Ancestral’ neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response , 1987, Journal of Comparative Physiology A.

[142]  R J Dunn,et al.  Function of NMDA receptors and persistent sodium channels in a feedback pathway of the electrosensory system. , 2001, Journal of neurophysiology.

[143]  E. Fortune,et al.  New techniques for making whole-cell recordings from CNS neurons in vivo. , 1996 .

[144]  N. Lemon,et al.  Conditional spike backpropagation generates burst discharge in a sensory neuron. , 2000, Journal of neurophysiology.

[145]  Joseph Bastian,et al.  Gain control in the electrosensory system: a role for the descending projections to the electrosensory lateral line lobe , 1986, Journal of Comparative Physiology A.

[146]  V. Han,et al.  Cell Morphology and Local Circuitry of the Central Lobes of the Mormyrid Cerebellum , 2002, Annals of the New York Academy of Sciences.

[147]  H. Zakon,et al.  Plasticity of electroreceptor tuning in the weakly electric fish,Sternopygus dariensis , 1983, Journal of comparative physiology.

[148]  L. Maler,et al.  Excitatory amino acid receptors at a feedback pathway in the electrosensory system: implications for the searchlight hypothesis. , 1997, Journal of neurophysiology.

[149]  M. Kawasaki,et al.  Neuronal circuitry for comparison of timing in the electrosensory lateral line lobe of the African wave-type electric fish Gymnarchus niloticus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[150]  J. Bastian,et al.  Dendritic modulation of burst-like firing in sensory neurons. , 2001, Journal of neurophysiology.

[151]  Carl D. Hopkins,et al.  On the Diversity of Electric Signals in a Community of Mormyrid Electric Fish in West Africa , 1981 .

[152]  Walter Heiligenberg,et al.  Labelling of electroreceptive afferents in a gymnotoid fish by intracellular injection of HRP: The mystery of multiple maps , 1982, Journal of comparative physiology.

[153]  C E Carr,et al.  A time-comparison circuit in the electric fish midbrain. II. Functional morphology , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[154]  W Heiligenberg,et al.  Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: The accommodation of two behaviors in one nucleus , 1988, The Journal of comparative neurology.

[155]  C. Bell,et al.  Neuronal responses to electrosensory input in mormyrid valvula cerebelli. , 1978, Journal of neurophysiology.

[156]  M. V. Bennett,et al.  Electroreceptors in mormyrids. , 1965, Cold Spring Harbor symposia on quantitative biology.

[157]  B. Grothe.  The evolution of temporal processing in the medial superior olive, an auditory brainstem structure , 2000, Progress in Neurobiology.

[158]  R. Fettiplace,et al.  The effects of low calcium on the voltage‐dependent conductances involved in tuning of turtle hair cells. , 1993, The Journal of physiology.

[159]  C. Bell,et al.  Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish: I. Morphology , 1989, The Journal of comparative neurology.

[160]  J Bastian,et al.  Plasticity in an electrosensory system. I. General features of a dynamic sensory filter. , 1996, Journal of neurophysiology.

[161]  L. Maler,et al.  Interaction of GABAB-mediated inhibition with voltage-gated currents of pyramidal cells: computational mechanism of a sensory searchlight. , 1998, Journal of neurophysiology.

[162]  J. Harlan Meyer,et al.  Behavioral responses of weakly electric fish to complex impedances , 1982, Journal of comparative physiology.

[163]  M. A. Friedman,et al.  Time coding in the midbrain of mormyrid electric fish. I. Physiology and anatomy of cells in the nucleus exterolateralis pars anterior , 1998, Journal of Comparative Physiology A.

[164]  J. Bastian.  Electrolocation: I. How the electroreceptors ofApteronotus albifrons code for moving objects and other electrical stimuli , 1981 .

[165]  C. Bell.  An efference copy which is modified by reafferent input. , 1981, Science.

[166]  C D Hopkins.  Eelectric communication in fish. , 1974, American scientist.

[167]  J. Bastian.  Electrolocation: II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells inApteronotus albifrons , 1981 .

[168]  Gabbiani,et al.  Encoding and processing of sensory information in neuronal spike trains , 1999, The Journal of experimental biology.

[169]  M H Ellisman,et al.  TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[170]  W. Metzner.  The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.