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Intrinsic and Synaptic Properties of Olfactory Bulb Neurons

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Intrinsic and Synaptic Properties of Olfactory Bulb Neurons INTRINSIC AND SYNAPTIC PROPERTIES OF OLFACTORY BULB NEURONS AND THEIR RELATION TO OLFACTORY SENSORY PROCESSING by RAMANI BALU Submitted in partial fulfillment of the requirements For the degree of Doctor of Philosophy Thesis Advisor: Dr. Ben W. Strowbridge Department of Neurosciences CASE WESTERN RESERVE UNIVERSITY May, 2007 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the thesis/dissertation of _________________Ramani Balu__________________________ Candidate for the ______________Ph.D._____________ degree *. (signed)_________Iain Robinson __________________________ (chair of committee) _______________Ben Strowbridge ________________________ _______________Ruth Siegel ____________________________ _______________Stefan Herlitze _________________________ _______________R. John Leigh __________________________ (date)____October 20, 2006______________ *We also certify that written approval has been obtained for any proprietary material contained therein. ii Table of Contents Table of Contents...............................................................................................................iii List of Figures..................................................................................................................... v Acknowledgements............................................................................................................ vi List of Abbreviations ........................................................................................................ vii Abstract.............................................................................................................................. ix Chapter 1 : Introduction...................................................................................................... 1 Anatomical Organization of the Mammalian Olfactory System .................................... 2 Synaptic Mechanisms of Mitral Cell Spike Patterning................................................... 4 Reciprocal dendrodendritic inhibition between mitral and granule cells ................... 5 Gating of dendrodendritic inhibition under normal physiological conditions............ 8 Regulation of action potential propagation in mitral and granule cell dendrites...... 10 Plasticity at dendrodendritic synapses ...................................................................... 12 Other synaptic mechanisms of mitral cell spike patterning...................................... 15 Intrinsic Mechanisms of Mitral Cell Spike Patterning ................................................. 18 Overview of Dissertation .............................................................................................. 21 Chapter 2 : Phasic Stimuli Evoke Precisely Timed Spikes in Intermittently Discharging Mitral Cells ....................................................................................................................... 29 Summary....................................................................................................................... 29 Introduction................................................................................................................... 30 Materials and Methods.................................................................................................. 32 Results........................................................................................................................... 34 Discussion..................................................................................................................... 41 Mechanisms of Spike Clustering and Phase Locking............................................... 44 Functional Implications for Odor Coding................................................................. 47 Chapter 3 : Opposing Inward and Outward Intrinsic Currents Control Rebound Discharges in Mitral Cells ................................................................................................ 65 Summary....................................................................................................................... 65 Introduction................................................................................................................... 67 Materials and Methods.................................................................................................. 70 Results........................................................................................................................... 72 Discussion..................................................................................................................... 80 Chapter 4 : Multiple Modes of Synaptic Excitation Onto Granule Cells of the Olfactory Bulb................................................................................................................................... 98 Summary....................................................................................................................... 98 Introduction................................................................................................................... 98 Experimental Procedures ............................................................................................ 102 Slice preparation and recording .............................................................................. 102 Two-Photon Imaging .............................................................................................. 104 Two-Photon Guided Microstimulation................................................................... 105 Imaging Synaptically Evoked Calcium Transients................................................. 106 DiI Injections .......................................................................................................... 106 Results......................................................................................................................... 109 iii Two distinct classes of excitatory inputs onto granule cells................................... 109 Distal and proximal excitatory synapses are functionally distinct.......................... 113 Do granule cells have silent synapses? ................................................................... 117 What is the source of the proximal excitatory input to granule cells?.................... 121 Discussion................................................................................................................... 125 Multiple synaptic mechanisms for activating GABAergic granule cells................ 127 Source of the proximal axo-dendritic input onto granule cells............................... 129 Implications for the long-term plasticity at dendrodendritic synapses ................... 131 Chapter 5 : Discussion .................................................................................................... 159 Intrinsic regulation of synaptic integration of excitatory inputs................................. 161 Rebound spike generation and the regulation of local inhibitory inputs on mitral cells ..................................................................................................................................... 162 The “sniff” as a fundamental unit of olfactory bulb processing ................................. 163 Intrinsic regulation of action potential backpropagation ............................................ 165 Synaptic mechanisms of mitral cell patterning........................................................... 169 Plasticity in the olfactory bulb .................................................................................... 172 Modulation of intrinsic currents and plasticity ........................................................... 172 Plasticity at dendrodendritic synapses ........................................................................ 173 Bibliography ................................................................................................................... 178 iv List of Figures Figure 1-1. Glomerular organization of sensory inputs in the olfactory bulb.................. 23 Figure 1-2. Local circuits and synaptic processing in the olfactory bulb ........................ 25 Figure 1-3. Ultrastructure of olfactory dendrodendritic synapses ................................... 27 Figure 2-1. Intermittent firing and subthreshold oscillations in olfactory bulb mitral cells ........................................................................................................................................... 49 Figure 2-2. Variability of clustered spike discharge timing in mitral cells ...................... 51 Figure 2-3. Variability in mitral cell firing patterns does not reflect initial conditions... 53 Figure 2-4. Transient repolarizations promote precise phase locking in mitral cells...... 55 Figure 2-5. Precise spike timing in mitral cells activated by phasic stimuli .................... 57 Figure 2-6. Different effects of first and second sEPSPs.................................................. 59 Figure 2-7. Disruption of precise spiking by 4-AP ........................................................... 61 Figure 2-8. 4-AP sensitive K+ currents regulate intermittent discharges in mitral cells . 63 Figure 3-1. Transient hyperpolarizing stimuli evoke rebound discharges in mitral cells.84 Figure 3-2. Voltage dependence of rebound spiking in mitral cells. ................................ 86 Figure 3-3. Subthreshold Na currents boost mitral cell responses to depolarizing stimuli and mediate rebound spiking...........................................................................................
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