The Neuroethology of Predation and Escape

Keith T. Sillar is Professor and Head of theSchool of Psychology & Neuroscience at the University of St Andrews, in Scotland. His research interests include neurology, neuroscience and amphibian neurology. Along with Dr Heitler, he teaches an exchange course on neuroethology in the US. Dr William J Heitler is a reader at the School of Biology, University of St Andrews in Scotland, where his research interests include the neurology of crayfish and other crustacea, and escape behavior as well as more general neurology and neuroscience. He teaches an exchange course on neuroethology in the US in conjunction with Professor Sillar. Laurence Picton is at the School of Psychology and Neuroscience at University of St Andrews, Scotland.

General Introduction, xi What this book is about, xiii How this book is organised, xv Who this book is for, xvi Acknowledgements, xvi References, xvii 1 Vision, 2 1.1 The electromagnetic spectrum, 3 1.2 Eyes: acuity and sensitivity, 5 1.2.1 Foveae, 6 1.3 Feature recognition and releasing behaviour, 8 1.4 Prey capture in toads, 9 1.4.1 Attack or avoid: worms and anti -worms , 9 1.4.2 Retinal processing, 11 1.4.3 Feature detector neurons, 12 1.4.4 Modulation and plasticity, 14 1.4.5 Toad prey capture: the insects fight back, 15 1.5 Beyond the visible spectrum, 16 1.5.1 Pit organs, 16 1.5.2 Thermotransduction, 20 1.5.3 Brain processing and cross- modal integration, 21 1.5.4 Behaviour, 22 1.5.5 Infrared defence signals, 25 1.6 Aerial predators: dragonfly vision, 27 1.6.1 Dragonfly eyes, 27 1.6.2 Aerial pursuit, 28 1.6.3 Predictive foveation, 29 1.6.4 Reactive steering: STMDs and TSDNs, 30 1.7 Summary, 31 Abbreviations, 32 References, 32 2 Olfaction, 36 2.1 Mechanisms of olfaction, 38 2.1.1 Detection and specificity, 38 2.1.2 Olfactory sub systems, 40 2.1.3 Brain processing, 41 2.2 Olfactory tracking and localisation, 41 2.3 Pheromones and kairomones, 45 2.3.1 Alarm pheromones, 45 2.3.2 Predator odours, 46 2.3.3 Dual purpose signals: the MUP family, 47 2.3.4 Parasites: when kairomones go bad!, 49 2.4 Summary, 50 Abbreviations, 51 References, 51 3 Owl Hearing, 54 3.1 Timing and intensity, 56 3.2 Owl sound localisation mechanisms, 58 3.3 Anatomy, 60 3.4 Neural computation, 61 3.4.1 The auditory map, 62 3.4.2 Early stage processing, 66 3.4.3 ITD processing, 69 3.4.4 IID processing, 76 3.5 Combining ITD and IID specificity in the inferior colliculus, 77 3.6 Audio -visual integration and experience -dependent tuning of the auditory map, 78 3.6.1 Audio -visual discrepancy can re -map the ICC -ICX connections, 80 3.6.2 Motor adaptation, 82 3.6.3 Age and experience matter!, 82 3.6.4 Cellular mechanisms of re -mapping, 82 3.7 Summary, 83 Abbreviations, 84 References, 85 4 Mammalian Hearing, 88 4.1 Spectral cues, 90 4.1.1 Neural processing of spectral cues, 90 4.2 Binaural processing, 92 4.2.1 IID processing, 93 4.2.2 ITD processing, 94 4.2.3 Calyx of Held, 99 4.3 Do mammals have a space map like owls?, 100 4.4 Comparative studies in mammals, 101 4.5 Summary, 102 4.5.1 Caveats, 102 Abbreviations, 102 References, 103 5 The Biosonar System of Bats, 106 5.1 Bat echolocation, 107 5.1.1 Why ultrasound?, 108 5.1.2 Range limits, 109 5.2 The sound production system, 109 5.2.1 Types of sound: CF and FM pulses, 110 5.2.2 Echolocation in predation: a three -phase attack strategy, 112 5.2.3 Duty cycle and pulse -echo overlap, 113 5.3 The sound reception system, 114 5.3.1 Bats have big ears, 114 5.3.2 Peripheral specialisations: automatic gain control and acoustic fovea, 115 5.4 Eco -physiology: different calls for different situations, 116 5.4.1 Target discovery, 117 5.4.2 Target range and texture, 118 5.4.3 Target location, 119 5.4.4 Target velocity: the Doppler shift, 119 5.4.5 Target identity: flutter detection, 121 5.4.6 Jamming avoidance response, 123 5.4.7 Food competition and intentional jamming, 123 5.5 Brain mechanisms of echo detection, 124 5.5.1 The auditory cortex, 125 5.5.2 Range and size analysis: the FM -FM area, 125 5.5.3 Velocity analysis: the CF -CF area, 128 5.5.4 Fine frequency analysis: the DSCF area, 130 5.6 Evolutionary considerations, 131 5.7 The insects fight back, 132 5.7.1 Moth ears and evasive action, 132 5.7.2 Bad taste, 133 5.7.3 Shouting back, 134 5.8 Final thoughts, 135 5.9 Summary, 136 Abbreviations, 137 References, 137 6 Electrolocation and Electric Organs, 140 6.1 Passive electrolocation, 142 6.1.1 Ampullary electroreceptors, 142 6.1.2 Prey localisation, 145 6.1.3 Mammalian electrolocation, 146 6.2 Electric fish, 148 6.3 Strongly electric fish, 151 6.3.1 Freshwater fish: the electric eel, 151 6.3.2 Marine fish: The electric ray, 156 6.3.3 Avoiding self -electrocution, 158 6.4 Active electrolocation, 158 6.4.1 Weakly electric fish, 158 6.4.2 Tuberous electroreceptors, 161 6.4.3 Brain maps for active electrolocation, 163 6.4.4 Avoiding detection, mostly, 164 6.4.5 Frequency niches, 166 6.4.6 The jamming avoidance response, 167 6.5 Summary, 174 Abbreviations, 175 References, 175 7 The Crayfish Escape Tail -Flip, 178 7.1 Invertebrate vs. vertebrate nervous systems, 179 7.2 Tail -flip form and function, 180 7.3 Command neurons, 182 7.4 Motor output, 184 7.4.1 Directional control, 184 7.4.2 Rectifying electrical synapses, 186 7.4.3 Depolarising inhibition, 188 7.4.4 FF drive and the segmental giant neuron, 189 7.4.5 Limb activity during GF tail -flips, 189 7.4.6 Tail extension, 190 7.4.7 Non -giant tail -flips, 190 7.5 Activation of GF tail -flips, 191 7.5.1 Coincidence detection, 193 7.5.2 Habituation and prevention of self -stimulation, 195 7.6 Modulation and neuroeconomics, 196 7.6.1 Mechanisms of modulation, 197 7.6.2 Serotonin modulation, 198 7.7 Social status, serotonin and the crayfish tail -flip, 198 7.7.1 Social status effects on tail -flip threshold, 199 7.7.2 Serotonin effects on tail -flip threshold depend on social status, 200 7.8 Evolution and adaptations of the tail -flip circuitry, 202 7.8.1 Penaeus: a unique myelination mechanism gives ultra -rapid conduction, 205 7.9 Summary, 208 Abbreviations, 208 References, 209 8 Fish Escape: the Mauthner System, 212 8.1 Fish ears and the lateral line, 214 8.1.1 Directional sensitivity, 215 8.2 Mauthner cells, 215 8.2.1 Biophysical properties, 217 8.3 Sensory inputs to M -cells, 218 8.3.1 Feedforward inhibition and threshold setting, 220 8.3.2 PHP neurons: electrical inhibition, 220 8.4 Directional selectivity and the lateral line, 222 8.4.1 Obstacle avoidance, 223 8.5 M -cell output, 223 8.5.1 Feedback electrical inhibition: collateral PHP neurons, 223 8.5.2 Spinal motor output, 224 8.5.3 Spinal inhibitory interneurons: CoLos, 224 8.6 The Mauthner system: command, control and flexibility, 226 8.7 Stage 2 and beyond, 230 8.8 Social status and escape threshold, 230 8.9 Adaptations and modifications of the M -circuit, 233 8.10 Predators fight back: the amazing tentacled snake, 235 8.11 Summary, 239 Abbreviations, 239 References, 240 9 The Mammalian Startle Response, 244 9.1 Pathologies, 246 9.2 Neural circuitry of the mammalian startle response, 248 9.3 Modulation of startle, 250 9.4 Summary, 250 Abbreviations, 251 References, 251 10 The Ballistic Attack of Archer Fish, 254 10.1 The water pistol, 255 10.2 Perceptual problems and solutions, 257 10.3 Learning to shoot, 260 10.4 Prey retrieval by archer fish, 261 10.4.1 Computing the landing point, 262 10.4.2 Orientation, 263 10.4.3 Dash to the target, 264 10.5 Summary, 264 References, 265 11 Catapults for Attack and Escape, 266 11.1 The bow and arrow, 268 11.2 Catapults require multi -stage motor programmes, 269 11.3 Grasshopper jumping, 270 11.3.1 Biomechanics, 270 11.3.2 The behaviour, 270 11.3.3 The hind legs, 271 11.3.4 The motor programme, 273 11.3.5 Directional control, 279 11.3.6 Evolution of the grasshopper strategy, 279 11.4 Froghoppers: the champion insect jumpers, 280 11.4.1 Ratchet locks, 282 11.4.2 Synchronisation, 282 11.5 Mantis shrimps, 284 11.5.1 Mantis shrimp catapults, 285 11.5.2 Cavitation bubbles, 287 11.6 Snapping (pistol) shrimps, 288 11.7 Multi -function mouthparts: the trap -jaw ant, 291 11.8 Prey capture with prehensile tongues, 293 11.8.1 The chameleon tongue: sliding springs and supercontracting muscles, 293 11.8.2 Salamander tongue projection, 297 11.9 Temperature independence of catapults, 300 11.10 Summary, 300 Abbreviations, 301 References, 301 12 Molluscan Defence and Escape Systems, 304 12.1 Squid jet propulsion, 306 12.1.1 Biomechanics, 306 12.1.2 Neural circuitry, 307 12.1.3 Jetting behaviour, 311 12.2 Inking, 312 12.2.1 Neuroecology of inking, 314 12.2.2 Neural circuitry of inking, 315 12.3 Cephalopod colour and shape control, 316 12.3.1 Chromatophores, 317 12.3.2 Iridophores, 319 12.3.3 Leucophores, 321 12.3.4 Photophores, 321 12.3.5 Body shape and dermal papillae, 322 12.4 Summary, 323 Abbreviations, 323 References, 323 13 Neurotoxins for Attack and Defence, 326 13.1 Cone snails, 328 13.1.1 The biology of cone snail envenomation, 329 13.1.2 Conopeptides, 333 13.1.3 The billion dollar mollusc, 340 13.1.4 Rapid conch escape, 341 13.2 The neuroethology of zombie cockroaches, 343 13.2.1 Sensory mechanisms of stinger precision, 344 13.2.2 Transient paralysis, 345 13.2.3 Intense grooming, 346 13.2.4 Docile hypokinesia, 346 13.3 Venom resistance, 347 13.3.1 Targeting pain pathways, 350 13.3.2 From pain to analgesia, 350 13.4 Summary, 352 Abbreviations, 352 References, 352 14 Concluding Thoughts, 356 14.1 The need for speed, 358 14.2 Safety in numbers, 360 14.3 The unbalancing influences of humankind, 361 References, 363 Index, 364