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Neuroethology in Neuroscience Why Study an Exotic Animal

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Neuroethology in Neuroscience or Why study an exotic animal Nobel prize in Physiology and Medicine 1973 Karl von Frisch Konrad Lorenz Nikolaas Tinbergen for their discoveries concerning "organization and elicitation of individual and social behaviour patterns". Behaviour patterns become explicable when interpreted as the result of natural selection, analogous with anatomical and physiological characteristics. This year's prize winners hold a unique position in this field. They are the most eminent founders of a new science, called "the comparative study of behaviour" or "ethology" (from ethos = habit, manner). Their first discoveries were made on insects, fishes and birds, but the basal principles have proved to be applicable also on mammals, including man. Nobel prize in Physiology and Medicine 1973 Karl von Frisch Konrad Lorenz Nikolaas Tinbergen Ammophila the sand wasp Black headed gull Niko Tinbergen’s four questions? 1. How the behavior of the animal affects its survival and reproduction (function)? 2. By how the behavior is similar or different from behaviors in other species (phylogeny)? 3. How the behavior is shaped by the animal’s own experiences (ontogeny)? 4. How the behavior is manifested at the physiological level (mechanism)? Neuroethology as a sub-field in brain research • A large variety of research models and a tendency to focus on esoteric animals and systems (specialized behaviors). • Studying animals while ignoring the relevancy to humans. • Studying the brain in the context of the animal’s natural behavior. • Top-down approach. Archer fish Prof. Ronen Segev Ben-Gurion University Neuroethology as a sub-field in brain research • A large variety of research models and a tendency to focus on esoteric animals and systems (specialized behaviors). • Studying animals while ignoring the relevancy to humans. • Studying the brain in the context of the animal’s natural behavior. • Top-down approach. דג חשמל נמוכי מתח Weakly electric fish Jamming avoidance response Neuroethology as a sub-field in brain research • A large variety of research models and a tendency to focus on esoteric animals and systems (specialized behaviors). • Studying animals while ignoring the relevancy to humans. • Studying the brain in the context of the animal’s natural behavior. • Top-down approach. Place Cells 1.5 m Neuroethology as a sub-field in brain research • A large variety of research models and a tendency to focus on esoteric animals and systems (specialized behaviors). • Studying animals while ignoring the relevancy to humans. • Studying the brain in the context of the animal’s natural behavior. • Top-down approach. Some classical models in neuroethology Neuroethology where to? • The field is moving away from the neuroethological approach by focusing on rodent models and neglecting all other species. • The field is moving towards neuroethology by studying directly the physiology of behavior and by addressing natural behaviors that are relevant to the mouse. •Sound localization •Sensory maps plasticity and development •Spatial attention •Multisensory integration Barn owls as model system for sound localization • Facial ruff serves as a sound amplifier Barn owls as model system for sound localization • Facial ruff serves as a sound amplifier • Asymmetric ears allow for an increased spatial resolution in the vertical plane Barn owls as model system for sound localization • Facial ruff serves as a sound amplifier • Asymmetric ears allow for an increased spatial resolution in the vertical plane • Comb-like structures at the leading edge of the wing reduce noise during flight Barn owls as model system for sound localization Facial ruff serves as a • sound amplifier Asymmetric ears allow for • an increased spatial resolution in the vertical plane Comb-like structures at the • leading edge of the wing reduce noise during flight Brain structures involved • in the analysis of sound are enlarged Performing a psychoacoustic experiment with an owl Sound-localization with free-field stimuli • The auditory localization cues: • ITD - horizontal ILD - vertical location producing ITD = 0 µsec location producing ITD = 100 µsec Precision of sound localization in barn owls may be as good as 3 deg which corresponds to 6-10 µs. Action Postsynaptic potential potentials These signals are the “language" of neural processing. Durations of events • Typical duration of action potential: 1ms • Typical duration of post-synaptic potentials: 5-10 ms • Precision of sound localization by interaural time difference: 6-10 µs What has to be explained is Factor of 500-1000 The principle of phase locking as a means to conserve time Sinusoidal signal Presumed resulting post- synaptic potential Registered signal in computer Note that in this example the response always occurs at a phase of 180 degrees. Phase locking in the barn owl Phase locking can be measured by plotting spike arrival times with respect to the period of the stimulus tone. 5 kHz Period 200 µs 9 kHz Period 111 µs spikes number of Stimulus phase in degrees Precision of phase locking is 35 µs at 5 kHz (Koeppl (1997)). Jefferess model (1948) Ai + Ni = Ac + Nc Ai − Ac = Ni − Nc ITD left ear Right ear Delay lines Does the brain computes ITDs as Jefferess suggested? Nucleus Laminaris / Medial Superior Olive - sites of binaural convergence Anatomical evidence for Jeffress model ITD curves in Nucleus Laminaris s) µ ITD( Response Time (ms) ITD (µs) SOUND LOCALIZATION GAZE CONTROL Forebrain Sensory/Association Archistriatum Areas (FEF) Thalamus Ovoidalis Rotundus (MGN) (Pulvinar) Inferior Inferior Optic Tectum Midbrain Colliculus Colliculus central n. external n. (SC) D R VLVp (LSO/DNLL) Brainstem Tegmentum LAM (MSO) Motor Nuclei left right for gaze control cochlear n. cochlear n. Response 20 +20 ILD(dB) 0 0 el V - -20 20 R20 L20 0 az Response -50 0 50 ITD (µs) +20 20 V ILD(dB) 0 el 0 - -20 20 R20 L20 0 az Response -50 0 50 ITD (µs) Visual and auditory maps in the OT Computational map Transducing Computing Integrating cues Associating with sound to auditory localization from specific external space action-potentials cues locations Sound Frequency Space tuned Frequency Intensity Binaural localization cues Time Side of ear Computational maps The matching problem location producing ITD = 0 µsec location producing ITD = 100 µsec Computational maps The matching problem location producing ITD = 0 µsec location producing ITD = 100 µsec Normal Immediate Effect Prism-adapted of Prisms Knudsen and Knudsen J Neurosci (1989) Effect of prism experience on auditory tuning Normal Immediate effect of prisms +20 A A V V 0 el -20 L20 R20 0 az Knudsen and Brainard, Science (1991) Effect of prism experience on auditory tuning Normal Immediate effect After 8 weeks of of prisms prism experience +20 A A A V V V 0 el -20 L20 R20 0 az Quantification of learning 1. Behavioral test 2. Physiological test Decline in learning with age 6 7 Knudsen, E. I. .Science.(1998) . Increased capacity for learning in adults that have had appropriate experience as juveniles 6 7 Knudsen, E. I. .Science.(1998) . Effects of juvenile experience on adult learning 6 7 Knudsen, E. I. .Science.(1998) . Incremental learning 170 110 60 230 Incremental learning Linkenhoker and Knudsen (2002) Nature Rich and lively experiences increase learning capacity in adults Bergan et al., Journal of Neuroscience (2005) Summary • Decline in learning with age • Increased capacity for learning in adults that have had appropriate experience as juveniles • Incremental training improves learning • Rich and lively experiences increase learning capacity in adults Where is the site of plasticity? Forebrain Sensory/Association Archistriatum Areas (FEF) Thalamus Ovoidalis Rotundus (MGN) (Pulvinar) Inferior Inferior Optic Tectum Midbrain Colliculus Colliculus central n. external n. (SC) VLVp (LSO/DNLL) Brainstem Tegmentum LAM (MSO) Motor Nuclei left right for gaze control cochlear n. cochlear n. Horizontal section through the tectal lobe Visual input from Retina and Forebrain c 00 r 00 0 200 20 ICC 400 ICX 400 OT r m l c Site of plasticity in the ICX Debello et al., J. Neurosci. 2001 After prism learning Visual input from Retina and Forebrain c 200 r 200 0 400 40 ICC 600 ICX 600 OT r m l c The instructive signal - Operates in the ICX - Visually based Where is the instructive signal coming from? BDA injection site in ICX 250 µm Topography of the OT-ICX projection Layer 8 BDA FG r l Restricted lesion of the optic tectum r l 500 µm How can a visually based instructive signal act in an auditory structure? Horizontal section through the tectal lobe Visual input from Retina and Forebrain c 00 r 00 0 200 20 ICC 400 ICX 400 OT r m l c bicuculline recording bic 0 iontophoresis barrels recording barrel rec 0 50 50 ICC 100 100 µsec 500 µm ICX OT r m l c Light responses in the ICX Visual Receptive Fields in the ICX ICX OT ICX OT 0 µm bic -150 µm ICX -300 µm OT -450 µm -600 µm Properties of visual responses in ICX - Arrive from the OT - Display spatially restricted visual receptive fields - Form a map of space - Align with auditory spatial representation Model gate ITD 1 Visual Input Visual Input ITD 2 ITD 3 ITD 1 Visual Input Visual Input ITD 2 ITD 3 Input Auditory ITD 1 Visual Input Visual Input ITD 2 ITD 3 ICX Optic Tectum Bimodal Stimulus light right ear left ear Visual and auditory interactions in the ICX auditory ITD visual auditory + visual Average 60 12 14 30 8 s) µ 10 A (spikes) A 0 - ITD ( AV 6 4 A (spikes) A -30 - AV 6 0 -60 50 100 150 200 -80 -60 -40 -20 0 20 40 60 80 Post stimulus time (ms) ITD (µs) Bimodal stimulus Normal Visual input ICC ICX OT Bimodal stimulus Normal With prisms Visual input Visual input ICC ICC ICX ICX OT OT Bimodal stimulus Normal With prisms Visual input Visual input ICC ICC ICX ICX OT OT Summary An inhibitory gate controls the flow of visual • information into the auditory system Summary • An inhibitory gate controls the flow of visual information into the auditory system • The visual signals are appropriate to serve as the instructive signal for auditory plasticity • Eric Knudsen Daniel Feldman Michael Brainard Will Debello Stanford University Peter Hyde Brie Linkenhoker Joe Bergan Hermann Wagner - AACHEN University.
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