THE NEURAL BASIS OF HEAD DIRECTION AND SPATIAL CONTEXT IN THE INSECT CENTRAL COMPLEX by ADRIENN G. VARGA Submitted in partial fulfillment of requirements For the degree of Doctor of Philosophy Advisor: Dr. Roy E. Ritzmann Department of Biology CASE WESTERN RESERVE UNIVERSITY May 2017 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the thesis/dissertation of Adrienn G. Varga Candidate for the Doctor of Philosophy degree*. Committee Chair: Hillel J. Chiel Committee Member: Roy E. Ritzmann Committee Member: Mark A. Willis Committee Member: Jessica L. Fox Committee Member: David Friel Date of Defense: November 18th, 2016 *We also certify that written approval has been obtained for any proprietary material contained therein. Copyright © by Adrienn G. Varga All rights reserved Dedication For my Family Table of Contents Thesis Summary ................................................................................................................ 1 Chapter 1: Introduction ................................................................................................... 3 Mammalian navigation circuits ................................................................................... 6 Adaptive navigation .................................................................................................... 6 Head direction cells .................................................................................................. 10 Sensory cues underlying the head direction signal ................................................. 13 Head direction network ............................................................................................ 16 Relationship with other networks in the navigation system .................................... 17 Neural control of insect navigation in the central complex ..................................... 19 Central complex anatomy ......................................................................................... 19 Cellular composition of the central complex ........................................................... 21 Directional sensory signal processing in the central complex ................................ 23 Selection and maintenance of behavior ................................................................... 26 Visual and spatial memory ....................................................................................... 29 Visual pattern recognition .................................................................................. 29 Detour paradigm and spatial working memory ................................................. 31 Visual place learning .......................................................................................... 32 The physiological correlates of orientation in the central complex ....................... 33 i Local Field Potentials .................................................................................................. 35 The origin and function of local field potentials ..................................................... 35 Local field potentials in mammalian navigation circuits ......................................... 37 Rats rely on theta rhythm to synchronize navigational circuits ............................. 38 Bat navigational network activity ............................................................................. 39 Local field potentials in the arthropod brain ........................................................... 41 Oscillations in the insect brain ................................................................................. 41 Crayfish central complex network activity............................................................... 42 Summary ...................................................................................................................... 44 Chapter 2: Cellular Basis of Head Direction and Contextual Cues in the Insect Brain ................................................................................................................................. 47 Summary ...................................................................................................................... 48 Introduction ................................................................................................................. 49 Materials and Methods ............................................................................................... 53 Surgical procedures .................................................................................................. 53 Recording procedures ............................................................................................... 54 Spike sorting and data analysis ................................................................................ 57 Results .......................................................................................................................... 61 Central complex neurons encode head direction .................................................... 61 Tuning characteristics of head direction encoding neurons .................................. 62 Head direction encoding CX neurons rely upon allothetic and/or idiothetic cues 67 Head direction coding persists even in the absence of visual landmarks .............. 73 Central complex units encode rotation direction history ........................................ 75 ii Discussion ..................................................................................................................... 79 Chapter 3: Modulation of Central Complex Local Field Potentials by Head Direction and Spatial Context........................................................................................ 85 Summary ...................................................................................................................... 86 Introduction ................................................................................................................. 87 Materials and Methods ............................................................................................... 92 Experimental Procedures ......................................................................................... 92 Experimental subjects ............................................................................................... 92 Recording procedures ............................................................................................... 93 Data analysis and statistics ....................................................................................... 95 Results .......................................................................................................................... 98 Description of spontaneous LFPs in the cockroach central complex .................... 98 Head direction modulation of central complex network activity .......................... 101 Delta-band activity encodes head direction independent of the underlying sensory cues .......................................................................................................................... 104 Sensory context does not affect relative response magnitudes in the delta-band 106 Sensory context modulates the average power of central complex network activity in the theta-, beta- and gamma-bands, but not in the delta-band ......................... 111 Discussion ................................................................................................................... 114 Chapter 4: Conclusion .................................................................................................. 120 Considerations of the neural basis of navigation ................................................... 121 iii Broad discussion of major findings and their significance to the field of neurobiology .............................................................................................................. 123 Single neurons and LFPs encode head direction in the insect CX ...................... 124 Single neurons and LFPs encode spatial context cues in the insect CX .............. 128 Conclusions and Future Directions ......................................................................... 130 Appendix ........................................................................................................................ 131 Bibliography .................................................................................................................. 135 iv List of Tables Chapter 2: Table 2.1: . Landmark rotation experiment results indicate that CX units utilize five sensory strategies when encoding head direction. ....................................................... 70 Chapter 3: Table 3.1: Summary of LFP analysis results. ........................................................... 114 v List of Figures Chapter 1: Figure 1.1: Schematic illustration of the neural circuitry underlying mammalian navigation and context discrimination. ........................................................................ 12 Figure 1.2: Schematic illustration of the cockroach brain and the central complex (CX). ............................................................................................................................ 21 Chapter 2: Figure 2.1: Experimental design and paradigms to test head direction coding in the cockroach. .................................................................................................................... 55 Figure 2.2: CX units encode head direction by changes in firing rate.