Commissural neurons of the electrosensory lateral line lobe of Apteronotus leptorhynchus: morphological and physiological characteristics

Extracellular injections of horseradish peroxidase were used to label commissural cells connecting the electrosensory lateral line lobes of the weakly electric fish Apteronotus leptorhynchus. Multiple commissural pathways exist; a caudal commissure is made up of ovoid cell axons, and polymorphic cells' axons project via a rostral commissure. Intracellular recording and labeling showed that ovoid cells discharge spontaneously at high rates, fire at preferred phases to the electric organ discharge, and respond to increased receptor afferent input with short latency partially adapting excitation. Ovoid cell axons ramify extensively in the rostro-caudal direction but are otherwise restricted to a single ELL subdivision. Polymorphic cells are also spontaneously active, but their firing is unrelated to the electric organ discharge waveform. They respond to increased receptor afferent activity with reduced firing frequency and response latency is long. Electrical stimulation of the commissural axons alters the behavior of pyramidal cells in the contralateral ELL. Basilar pyramidal cells are hyperpolarized and nonbasilar pyramidal cells are depolarized by this type of stimulation. The physiological results indicate that the ovoid cells participate in common mode rejection mechanisms and also suggest that the ELLs may function in a differential mode in which spatially restricted electrosensory stimuli can evoke heightened responses.

[1]  T Szabo,et al.  Electroreceptor mechanisms in a high-frequency weakly electric fish, Sternarchus albifrons. , 1965, Journal of neurophysiology.

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

[3]  J. New Medullary electrosensory processing in the little skate , 1990, Journal of Comparative Physiology A.

[4]  L. Maler,et al.  Gap junction protein in weakly electric fish (gymnotide): Immunohistochemical localization with emphasis on structures of the electrosensory system , 1989, The Journal of comparative neurology.

[5]  Walter Heiligenberg,et al.  Sensory control of behavior in electric fish , 1991, Current Opinion in Neurobiology.

[6]  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.

[7]  A. Fessard,et al.  Physiology of Electroreceptors , 1974 .

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

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

[10]  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.

[11]  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.

[12]  Professor Dr. Bernd Kramer Electrocommunication in Teleost Fishes , 1990, Zoophysiology.

[13]  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.

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

[15]  Leonard Maler,et al.  The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus , 2004, Anatomy and Embryology.

[16]  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.

[17]  L. Maler,et al.  The posterior lateral line lobe of certain gymnotoid fish: Quantitative light microscopy , 1979, The Journal of comparative neurology.

[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]  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.

[20]  E. Batschelet Circular statistics in biology , 1981 .

[21]  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.

[22]  J. Dye,et al.  Dynamics and stimulus-dependence of pacemaker control during behavioral modulations in the weakly electric fish,Apteronotus , 1987, Journal of Comparative Physiology A.

[23]  Leonard Maler,et al.  Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis , 1993 .

[24]  Joseph Bastian,et al.  Morphological correlates of pyramidal cell adaptation rate in the electrosensory lateral line lobe of weakly electric fish , 1991, Journal of Comparative Physiology A.

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

[26]  J. Bastian,et al.  The role of amino acid neurotransmitters in the descending control of electroreception , 1993, Journal of Comparative Physiology A.

[27]  S. Matsakis Growth of Clytia spp. hydromedusae (Cnidaria, Thecata): effects of temperature and food availability , 1993 .

[28]  Walter Heiligenberg,et al.  Behavior of Mormyridae , 1986 .

[29]  J. L. Larimer,et al.  Sensory feedback from electroreceptors to electromotor pacemaker centers in gymnotids. , 1968, The American journal of physiology.

[30]  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.

[31]  C E Carr,et al.  Efferent projections of the posterior lateral line lobe in gymnotiform fish , 1982, The Journal of comparative neurology.

[32]  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 .

[33]  L. Maler,et al.  An atlas of the brain of the electric fish Apteronotus leptorhynchus , 1991, Journal of Chemical Neuroanatomy.

[34]  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.

[35]  D. Bodznick,et al.  Properties of Medullary Interneurons of the Skate Electrosense Provide Evidence for the Neural Circuitry Mediating Ventilatory Noise Suppression. , 1991, The Biological bulletin.

[36]  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.

[37]  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.

[38]  Eric I. Knudsen,et al.  Spatial aspects of the electric fields generated by weakly electric fish , 1975, Journal of comparative physiology.