Central organization of the electrosensory system in the paddlefish (Polyodon spathula)

The central connections of the electrosensory system were studied in the paddlefish Polyodon spathula by injecting biotinylated dextran amines into the dorsal octavolateral nucleus (DON), the cerebellum, and the mesencephalic tectum. The sole target of primary electrosensory fibers is the ipsilateral dorsal octavolateral nucleus. The principal neurons ascending from this nucleus project to the torus semicircularis, the lateral mesencephalic nucleus, and the mesencephalic tectum. The mesencephalic tectum projects back to the nucleus preeminentialis, which, in turn, projects to the cerebellar auricles and to the DON. The auricles are the main source of parallel fibers in the cerebellar crest ventral to the DON. The DON also receives input from the contralateral DON. These descending feedback loops are very similar to those of other electrosensory fishes. However, the paddlefish is unique in having three mesencephalic targets of electrosensory information. It is the only bony fish known to have extensive projections directly to the mesencephalic tectum and to a lateral mesencephalic nucleus in addition to the torus semicircularis. J. Comp. Neurol. 446:25–36, 2002. © 2002 Wiley‐Liss, Inc.

[1]  Ad. J. Kalmijn,et al.  The Detection of Electric Fields from Inanimate and Animate Sources Other Than Electric Organs , 1974 .

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

[3]  David Bodznick,et al.  Segregation of electroreceptive and mechanoreceptive lateral line afferents in the hindbrain of chondrostean fishes , 1985, Brain Research.

[4]  David Bodznick,et al.  SUPPRESSION OF COMMON MODE SIGNALS WITHIN THE ELECTROSENSORY SYSTEM OF THE LITTLE SKATE , 1992 .

[5]  Ad. J. Kalmijn,et al.  Hydrodynamic and Acoustic Field Detection , 1988 .

[6]  W. Chavin The Physiology of Fishes , 1957, The Yale Journal of Biology and Medicine.

[7]  G. Roth,et al.  Tectal activation of premotor and motor networks during feeding in salamanders. , 1994, European journal of morphology.

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

[9]  Frank Moss,et al.  Use of behavioural stochastic resonance by paddle fish for feeding , 1999, Nature.

[10]  H. F. Nachtrieb The primitive pores of Polyodon spathula (Walbaum) , 1910 .

[11]  David F. Russell,et al.  The paddlefish rostrum functions as an electrosensory antenna in plankton feeding , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  Northcutt Rg,et al.  Medullary and Mesencephalic Pathways and Connections of Lateral Line Neurons of the Spiny Dogfish Squalus acanthias , 1988 .

[13]  D. Bodznick,et al.  The Specificity of an Adaptive Filter That Suppresses Unwanted Reafference in Electrosensory Neurons of the Skate Medulla. , 1993, The Biological bulletin.

[14]  Jie He,et al.  Afferent and Efferent Connections of Nucleus praeeminentialis in the Channel Catfish: A Reevaluation , 1998, Brain, Behavior and Evolution.

[15]  T. Szabó,et al.  Principles of electrolocation and jamming avoidance in electric fish. A neuroethological approach , 1978 .

[16]  Ruben Budelli,et al.  Electric fish measure distance in the dark , 1998, Nature.

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

[18]  John C. Montgomery,et al.  Noise cancellation in the electrosensory system of the thornback ray; common mode rejection of input produced by the animal's own ventilatory movement , 2004, Journal of Comparative Physiology A.

[19]  W. Smeets,et al.  The central nervous system of cartilaginous fishes: a neuro-anatomical study based on normal and experimental material , 1983 .

[20]  Jelle Atema,et al.  Sensory Biology of Aquatic Animals , 1988, Springer New York.

[21]  Joseph Bastian,et al.  Vision and electroreception: Integration of sensory information in the optic tectum of the weakly electric fishApteronotus albifrons , 1982, Journal of comparative physiology.

[22]  A. Kalmijn,et al.  Electric and magnetic field detection in elasmobranch fishes. , 1982, Science.

[23]  A. Kalmijn,et al.  The electric sense of sharks and rays. , 1971, The Journal of experimental biology.

[24]  G. Emde Orientation in the dark: brain circuits involved in the perception of electric signals in mormyrid electric fish. , 1999 .

[25]  J. McKENDRICK,et al.  The Central Nervous System of Vertebrates , 1909, Nature.

[26]  R. L. Boord,et al.  Medullary and mesencephalic pathways and connections of lateral line neurons of the spiny dogfish Squalus acanthias. , 1988, Brain, behavior and evolution.

[27]  R. Northcutt,et al.  Evolution of the Vertebrate Central Nervous System: Patterns and Processes , 1984 .

[28]  R. L. Boord,et al.  Ascending lateral line pathways to the midbrain of the clearnose skate, Raja eglanteria , 1982, The Journal of comparative neurology.

[29]  H. Vanegas,et al.  Electrophysiological and Behavioral Aspects of the Teleostean Optic Tectum , 1984 .

[30]  J. Albert,et al.  Tectal Fiber Connections in a Non-Teleost Actinopterygian Fish, the Sturgeon Acipenser , 1999, Brain, Behavior and Evolution.

[31]  A. Klimley,et al.  Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic field , 1993 .

[32]  A. Niida,et al.  An extensive projection of fish dorsolateral tegmental cells to the optic tectum revealed by intra-axonal dye marking , 1984, Neuroscience Letters.

[33]  D. Bodznick,et al.  Distinct but overlapping populations of commissural and GABAergic neurons in the dorsal nucleus of the little skate, Raja erinacea. , 1997, Brain, behavior and evolution.

[34]  David Bodznick,et al.  Suppression of Ventilatory Reafference in the Elasmobranch Electrosensory System: Medullary Neuron Receptive Fields Support a Common Mode Ejection Mechanism , 1992 .

[35]  David Bodznick,et al.  HINDBRAIN CIRCUITRY MEDIATING COMMON MODE SUPPRESSION OF VENTILATORY REAFFERENCE IN THE ELECTROSENSORY SYSTEM OF THE LITTLE SKATE RAJA ERINACEA , 1993 .

[36]  W. Smeets Efferent tectal pathways in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata , 1981, The Journal of comparative neurology.

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

[38]  J. Sisneros,et al.  Electrosensory optimization to conspecific phasic signals for mating , 1995, Neuroscience Letters.

[39]  S. Sharma,et al.  Organization of extrinsic tectal connections in goldfish (Carassius auratus) , 1981, The Journal of comparative neurology.

[40]  H. W. Lissmann,et al.  Continuous Electrical Signals from the Tail of a Fish, Gymnarchus niloticus Cuv. , 1951, Nature.

[41]  D. Bodznick,et al.  An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish , 1994, Neuroscience Letters.

[42]  A. Kalmijn Experimental Evidence of Geomagnetic Orientation in Elasmobranch Fishes , 1978 .

[43]  R. L. Boord,et al.  Central Lateral Line and Auditory Pathways: A Phylogenetic Perspective , 1984 .