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Evolvability and Sensor Evolution University of Birmingham 25 April 2003

Evolvability and Sensor Evolution University of Birmingham 25 April 2003. Electroreception: Functional, evolutionary and information processing perspectives. Mark E. Nelson Beckman Institute Univ. of Illinois, Urbana-Champaign. Overview. Background on electric fish

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Evolvability and Sensor Evolution University of Birmingham 25 April 2003

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  1. Evolvability and Sensor EvolutionUniversity of Birmingham25 April 2003 Electroreception: Functional, evolutionary and information processing perspectives Mark E. Nelson Beckman Institute Univ. of Illinois, Urbana-Champaign

  2. Overview • Background on electric fish • Functional considerations • mechanosensory signals (lateral line) • low-frequency electrosensory (passive) • high-frequency electrosensory (active) • Evolution and development • developmental clues • evolution and evolvability • Information processing considerations • shared spatial signal characteristics • topographic maps • shared mechanisms for improving S/N

  3. Distribution of electric fish

  4. Modes of electroreception • Passive (fields from external sources) • Animate (bioelectric, gills, muscle, heart) • Inanimate (electrochemical, geomagnetic) • Sharks, skates, rays, catfish, all electric fish • Active (perturbations to fish’s own field) • Animate (other animals, predators, prey) • Inanimate (any object with an electrical conductivity differing from the water) • All weakly electric fish (knifefish, elephant-nose) • Some strongly electric fish (electric eel)

  5. Electroreceptor Organ Morphology

  6. Apteronotus albifrons (black ghost knifefish)

  7. Functional considerations Active Electrolocation

  8. Receptor distribution ~14,000 tuberous electroreceptor organs Low freq E mechano MacIver, from Carr et al., 1982

  9. Principles of electrolocation • millivolt signal amplitudes • audio frequency range (carrier freq ~ 1 kHz) • amplitude modulation (AM depth ~ 1-10%)

  10. Prey-capture video analysis

  11. Fish Body Model

  12. Motion capturesoftware

  13. Sample High-Freq. Electrosensory Image

  14. Functional considerations Physical Characteristics of the Target

  15. Daphnia signal characteristics • Mechanosensory stimuli • Low-frequency bioelectric fields • Perturbations to the fish’s high-frequency electric field Daphnia 1 mm

  16. Mechanosensory • Kirk, K.L., Water flows produced by Daphnia… Limnol. Oceanogr 1985. • Jerky propulsion using main antennae • Fast power stroke – Daphnia moves up • Slow recover phase – Daphnia sinks • Normal swimming 1-3 antennal beats s-1 • Escape bursts up to 23 beats s-1 • Typical flows near antennae ~ 10 mm s-1

  17. Bioelectric fields (low freq)W. Wojtenek, L. Wilkens, et al.Univ. of Missouri, St. Louis • Daphnia produce both DC and low-frequency AC bioelectric fields • DC: up to 1000 mV, orientation dependent • AC: 10-100 mV, 3-15 Hz

  18. Bioelectric fields (low freq)Wojtenek, Wilkens, et al. DC

  19. Bioelectric fields (low freq)Wojtenek, Wilkens, et al. AC

  20. Active Electrolocation

  21. Daphnia Perturbation • Voltage perturbation at skin Df: prey volume fish E-field at prey electrical contrast distance from prey to receptor Worst case: prey is invisible, Df = 0 Best case: prey is perfect conductor

  22. Evolutionary and developmental considerations Electrosensory / Mechanosensory Relationships

  23. |Dprey| is independent of rA(r) ~ 1/r2 2 Low freq E Neuromasts respond to Dp between pores Dp(r) ~ 1/r3 3 mechano |Efish | falls off with rDf(r) ~ 1/r3 – near fieldDf(r) ~ 1/r5 - far field 3-5 High freq E Peak dipole amplitude Receptor activation A(r) 1/rp

  24. Multimodal contributions Electrosensory (active) Electrosensory (passive) Mechanosensory lateral line

  25. ~ 250 mechanosensory receptor organs mechano Coombs ~ 700 passive electrosensory receptor organs Low freq E Carr et al. 1982 ~ 14,000 active electrosensory receptor organs bb High freq E MacIver, from Carr et al., 1982 ApteronotusReceptor number ApteronotusReceptor distribution

  26. Mechanosensory Sense Organ Morphology Coombs et al., 1988

  27. Ontongeny Jørgensen, 1989

  28. Phylogeny Jørgensen, 1989

  29. Information processing considerations Central processing of Electrosensory and Mechanosensory Signals

  30. Spatiotemporal Filtering in ELL Central Processing in the ELL

  31. Spatiotemporal processing in the ELL

  32. Conclusions I: • General insights into evolution of the electric sense • although it may seem exotic to us, electric sensing was an early discovery in the course of vertebrate evolution • the electrosensory system is closely related to the lateral line system of fish and hearing and balance in terrestrial animals • receptor cell and receptor organ plasticity seem to be central to evolvability of different modalities and submodalities

  33. Conclusions II: • Information processing in electrosensory & mechanosensory systems • share similar spatial processing properties • dipole nature of the stimuli • topographic maps • differ in temporal processing (different time scales, different propagation delays) • mechanosensory 1 Hz vs. electrosensory 1000 Hz • speed of sound vs. speed of light • share similar neural mechanisms for improving signal-to-noise ratios • spatiotemporal integration • adaptive noise suppression

  34. Acknowledgements • Sheryl Coombs, collaborator at Loyola • Malcolm MacIver (former grad student, new faculty member at Northwestern) • Ruediger Krahe, Niklas Ludtke, Ling Chen, Kevin Christie, Jonathan House (current Nelson lab members) • NIMH and NSF

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