Hippocampal Theta-Related Properties of the Basal Ganglia

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Hippocampal Theta-Related Properties of the Basal Ganglia University of Calgary PRISM: University of Calgary's Digital Repository Graduate Studies Legacy Theses 2001 Hippocampal theta-related properties of the basal ganglia Hallworth, Nicholas E. Hallworth, N. E. (2001). Hippocampal theta-related properties of the basal ganglia (Unpublished master's thesis). University of Calgary, Calgary, AB. doi:10.11575/PRISM/12950 http://hdl.handle.net/1880/40798 master thesis University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca THE UNIVERSITY OF CALGARY Hippacampal Theta-Related Properties of the Basal Ganglia by Nicholas E. Hallworth A THESIS SUBMlTTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE DEPARTJMENT OF PSYCHOLOGY CALGARY, ALBERTA JANUARY, 2001 O Nicholas E. Hallworth National Liimry Bibliothmue nationale 1*1 ofcam& du Canada Acquisitions and Acquisitions et Bibliographic Sewices services bibliographiques 395 Wellington Street 395. nm Wellington OttawaON KlAON4 O(Lawa0N KlAW Canada Canada The author has granted a non- L'auteur a accorde une licence non exclusive licence allowing the exclusive pennettant a la National Library of Canada to Bbliotheque nationale du Canada de reproduce, loan, distribute or sell reproduire, prster, distribuer ou copies of this thesis in microform, vendre des copies de cette thbe sous paper or electronic fonnats. la forme de microfichelfilm, de reproduction sur papier ou sw fonnat eectronique. The author retains ownershtp of the L'auteur conserve la propndte du copyright in this thesis. Neither the droit d'autew qui protkge cette these. thesis nor substantial extracts fiom it Ni la these ni des extraits substantiels may be printed or otherwise de celle-ci ne doivent etre imprimis reproduced without the author's ou autrement reproduits sans son permission. autonsation. Abstract Using the electrical activity recorded fiom these structures as a guide, the present study examined interactions between the hippocampal formation and the basal ganglia. In urethane anaesthetized rats, extracellular recordings were made for cells located in the basal ganglia during hippocampal electroencephalographic desynchrony (LIA) and spontaneously occurring and/or sensory induced hippocampal electrencephalographic synchrony (theta). A large proportion of these neurons were considered to have discharge profiles that were related to the simultaneously recorded hippocampal field state. The routes through which theta-related cells of the basal ganglia interact with the hippocampus were assessed. Further investigation revealed two distinct populations of theta-related cells in the basal ganglia: those that either contribute or monitor ascending sensory information which acts to synchronize the field activity recorded fiom the hippocampus, and those that receive descending information from the septohippocampal system which potentially could influence motor output. Acknowledgements First and foremost, I must acknowledge Dr. Brian Bland Simply put, he has made ". ..an electrophysiologist out of me. ..". Dr. Bland's enthusiasm for theta research is infectious, and the dedication he has for his work makes him an extraordinary scientist, He has been a great mentor and friend Cheryl Bland has also been a tremendous inspiration. Her generosity, opemess, and warmth are incomparable, making my experience both inside and outside the laboratory a joy. Together, the Blands' loyal and dedicated, but also celebratory, attitude has profoundly influenced the manner in which I approach every day. I had the fortune to interact wrth many significant individuals throughout my time in the Bland laboratory. From the beginning I received thorough training from Darren Scarlett and Dr. Yasuhiro Hanada Later, additional help came from Drs. Kiyohisa Natsume and Jan Konopacki. The techniques I gleaned fiom these scientists were invaluable. Analytical help came from a number of sources. I am indebted to Dr. Charles Scialfa for his patience and willingness to discuss exmental designs and methods. I received additional help in this area from Dr. Lome Sulsky and Matt Scott. I was very fortunate to have Dr. Jos Eggemout as an instructor. He was always ready to discuss my results and suggest analytical options. I gratefully acknowledge Dr. Yoshiki Kaneoke for the provision of the burst and oscillation detection algorithms. Fortunately, I was able to review and compare these techniques with Dr. Kaneoke, Peter Magill, and Dr. Mark Bevan I am indebted to Dr. Cam Teskey for having read and revised my manumipt. Furthermore, Dr. Teskey was a most valuable source of criticism, always forcing me to consider my work fiom different viewpoints. Drs, Bob Sainsbury, Marshall Wibo, and Richard Dyck provided similar services, challenging me to cogtemplate my findings within a wider neuroscientific context. I was always able to discuss my work with Audny Dypvik, Marie Monfils, Craig Brown, Isaac Bogoch, Sam Lazareck, Ryan Cooper, Greg Neehly, Danen Fogg, Chris Wright, Peter Rilstone, and Parneet Cheema. These conversations were always fruitfid and motivating. Finally, I would like to acknowledge my parents, Michael and Annette Hallworth. Your Love and support are immeasurable. Thank you This work is dedicated to my grandparents, Herbert and Beryl Hallworth. Without you, none of this would be possible. PH-SUM complex ............................. 27 Bfstinstem .................................... 28 Pharmacology ....................................... 29 Hippocampa1 field activity ....................... 29 Hippocampal cell activity ........................ 30 Medial septum ................................. 32 PH-SUMcomplex .............................. 34 Brainstem .................................... 35 Function of hippocampal theta ................................ 35 The basaI ganglia .......................................... 37 Structure and fiber connections of the basal ganglia ............... 38 Anatomy of the caudate-putamen ........................ 39 Anatomy of the globus pallidus ......................... 39 Anatomy of the substantia nigra ......................... 40 Pars reticdata ................................. 40 Pars compacta ................................. 41 Circuitry of the basal ganglia ................................. 41 Afferent connections .................................. 41 CorticomiataI projections ........................ 41 Thalamostn'atal projections ....................... 42 Nigrostriatal projections ......................... 42 Other ascending afferent projections ............... 43 Efferent connections .................................. 43 Striatopllidd projections ........................ 43 Striatonigral projections ......................... 44 Connections of the subthdairnc nucleus ............ 44 Projections fiom the globus pallidus ................ 45 Projections fiom the enteropeduncular nucleus and the pars reticulata of the substantia nigra ........ 45 The direct and indirect pathways ........................ 46 The basal ganglia aad motor control ............................ 47 Unit electrophysology of the basal ganglia ................ 47 Interactions between the basal ganglia and the ascending hippocampal synchronizing systems ........................... 51 Anatomy ........................................... 51 EIectrophysioIogy .................................... 53 Objectives and hypotheses ................................... 56 Methods-Experiment one ................................................ 59 Objectives ..................................................... 59 Subjects ....................................................... 59 Surgery ....................................................... 60 Data acquisition ................................................ 63 Data analysis ................................................... 67 Results-Experiment one ................................................. n viii Histology ...................................................... 77 Classification ................................................... 78 Distriiution .................................................... 127 Discussion-Experiment one ............................................. 135 Methods-Experiment two ............................................... 153 Objectives ..................................................... 153 Subjects ....................................................... 154 Surgery ....................................................... 154 Data acquisition ................................................ 162 Data analysis .................................................. 164 Results-Experiment two ................................................ 164 SN stimulation ................................................. 164 GP stimulation ................................................. 171 CPu stimulation ................................................ 178 Discussion-Experiment two ............................................. 188 Methods-Experiment three .............................................. 195 Objectives ..................................................... 195 Subjects ...................................................... 196 Surgery
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