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Computational neuroethology: linking neurons, networks and behavior Mark E. Nelson Beckman Institute Univ. of Illinois, Urbana-Champaign TALK OUTLINE Multiscale modeling in computational neuroethology Model system - weakly electric fish Modeling strategies Level Level Level Level I: II: III: IV: Summary Behavior Sensory physics Single neurons Local networks Multiscale Organization of the Nervous System Delcomyn 1998 Organism 1m Brain/CNS 10 cm Brain maps 1 cm Networks 1 mm Neurons 100 mm Synapses 1 mm Molecules 1Å Churchland & Sejnowski 1988 Neuroethology: Neural Basis of Behavior Organism Neural Integration Sensory Processing Brain Motor Control Body Sensors Effectors Environment Delcomyn 1998 Neuroethology of Electrolocation Big picture: What are the neural mechanisms and computational principles of active sensing? Small picture: How do weakly electric fish capture prey? What computations take place in the CNS during prey capture behavior? BACKGROUND Weakly Electric Fish Distribution of Electric Fish Black ghost knifefish (Apteronotus albifrons) Electroreceptors mechano ~15,000 tuberous electroreceptor organs 1 nerve fiber per electroreceptor organ up to 1000 spikes/s per nerve fiber MacIver, from Carr et al., 1982 Ecology & Ethology of A. albifrons inhabits tropical freshwater rivers and streams in South America nocturnal; hunts at night for aquatic insect larvae and small crustaceans in turbid water uses electric sense for prey detection, navigation, social interactions ribbon fin propulsion – forward/reverse/hover Self-generated Electric Field Principle of active electrolocation Prey-capture Behavior Daphnia magna (water flea) 1 mm BEHAVIOR Electrosensory-mediated Prey capture behavior Prey-capture video analysis Prey capture behavior Fish Body Model Motion capture software Motion capture software MOVIE: prey capture behavior Rapid reversal marks putative time-of-detection Velocity Profile (N=116) Acceleration Profile (N=116) Zero-crossing in acceleration is used as detection time Distribution of detection points Front view Side view Active motor strategies: Dorsal roll toward prey Neuroethology: Neural Basis of Behavior Organism Neural Integration Sensory Processing Brain Motor Control Body Sensors Effectors Environment Delcomyn 1998 PHYSICS of electrosensory image formation Electrosensory Image Reconstruction Estimating Daphnia signal strength Voltage perturbation at skin Df: fish E-field at prey prey volume electrical contrast E fish r 3 1 prey / water a Df 3 1 2 / r prey water distance from prey to receptor THIS FORMULA CAN BE USED TO COMPUTE THE SIGNAL AT EVERY POINT ON THE BODY SURFACE Reconstructed Electrosensory Image (Df) Electrosensory Images ELECTROPHYSIOLOGY of primary sensory afferents Electroreceptors mechano ~15,000 tuberous electroreceptor organs 1 nerve fiber per electroreceptor organ MacIver, from Carr et al., 1982 Neural coding in electrosensory afferent fibers Probability coding (P-type) afferent spike trains Phead = 0.333 Phead = 0.337 Phead = 0.333 00010101100101010011001010000101001010 Model of primary afferents Brandman & Nelson Neural Comp. 14, 1575-1597 (2002) ELECTROPHYSIOLOGY of CNS electrosensory neurons ELL Circuitry ELL histology Compartmental Modeling Compartmental Modeling Hodgkin-Huxley Model for voltage-dependent conductances Compartmental Modeling Hodgkin-Huxley Model for voltage-dependent conductances I ion g Na m3h(Vm ENa ) g K n 4 (Vm EK ) g L (Vm EL ) dm m (V )(1 m) m (V )m dt dh h (V )(1 h) h (V )h dt dn n (V )(1 n) n (V )n dt ELL pyramidal cell ELECTROPHYSIOLOGY of electrosensory networks Central Processing in the ELL Spatiotemporal processing in 3 parallel ELL maps Centromedial map Space: small RFs Time: low-pass Primary Electrosensory Afferents Centrolateral map Space: med. RFs both Time: band-pass Lateral map Space: large RFs Time: high-pass Multiresolution filtering in the CNS Neuroethology: Neural Basis of Behavior Organism Neural Integration Sensory Processing Brain Motor Control Body Sensors Effectors Environment Delcomyn 1998 Acknowledgements Malcolm MacIver Noura Sharabash Relly Brandman Jozien Goense Rama Ratnam Rüdiger Krahe Ling Chen Kevin Christie Jonathan House NIMH and NSF