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Spatial Cells in the Subiculum; Influence of Boundary Manipulations

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Spatial Cells in the Subiculum; Influence of Boundary Manipulations Spatial cells in the Subiculum; Influence of boundary manipulations Sarah Stewart BSc (Hons) MSc Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds Institute of Psychological Sciences, Faculty of Medicine and Health March 2013 The candidate confirms that the work submitted is her own and that appropriate credit has been given where reference has been made to the work of others. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. The right of Sarah Stewart to be identified as the Author of this work has been asserted by her in accordance with the Copyright, Designs and Patents Act 1988. © 2012 The University of Leeds and Sarah Stewart i Acknowledgements I would like to dedicate this thesis to my little cousin Beth. Beth was a pragmatic and curious girl who was fascinated by everything. By the age of 10 she had already decided that when she grew up she wanted to be a scientist like me. Last year we lost Beth to Leukaemia. I would therefore like to dedicate this work to Beth, who we all miss and who will always be in my heart. I would like to give thanks to Dr Colin Lever. I could not have asked for a more enthusiastic and inspirational supervisor. I am grateful to Colin for encouraging my interest in science and for taking me on as PhD student. Colin’s maintained enthusiasm meant that after every meeting I was always left excited and with fresh ideas, for that I am indebted. Further I would like to thank Colin’s wife Kate and his children Rose and Moss for putting up with my home visits for our out of hours supervisory meetings. On a light note, I would also like to thank Colin for not laughing in my face when I first told him I thought I had recorded subicular grid cells. I would also like to thank Professor John Rodgers for his unerring support and for his time and assistance over the years. After Colin had moved from Leeds to Durham John became my first supervisor and took over all of Colin’s administrative roles. For that and for keeping me organised I will be eternally grateful. There are also many other people who have helped with various aspects of my PhD. I would like to thank Neil, Lisa, Mark, Mark and Rob for their assistance and help with all lab-related things. A big thank you also goes to Vincent Douchamps for helping me set up my lab and for constant technical support. I would also like to thank my Colleagues at UCL for help with histology and analyses. Ali Jeewajee, Tom Wills and Francesca Cacucci I would like to thank for their help with the grid cell analyses and useful discussion. Particular thanks must be given to Stephen Burton, who not only was of great help with histology, but also entertained and looked after me during all of my trips to UCL. I would like to also give special thanks to Brian and Agnes Wallwork, for firstly hand-making all of my testing environments, and for secondly becoming treasured friends. Brian and Agnes’ friendship and correspondence has continued to make me smile since our very first meeting three years ago. I would like to give thanks to the friends I have made during my time at IPS; Neil Boyle, Ian Flatters, Emily Norris, Rebecca Graber, Nathan Illman, Anna Rossiter and Sarah Smith. It has been a pleasure working with them and I am so thankful for their support and companionship. In particular I would like to thank Fay Twiston-Davies, Suzi Morson and Christine Wells. I give specific thanks to Fay and Christine for being my lab companions. Both of whom kept me smiling during the long hours of testing, and often kept me from going mad during the dark trials. I would like to thank Suzi for her unofficial role as my PA. Truly without her I would have never got anything done. Thank you also to Suzi and Christine for the continuous supply of wine and cheese nights, without you my PhD would have been impossible. It has been an emotional journey the last few years and I am so grateful and thankful that we were together through it. Lastly I would like to thank my family for their encouragement and for taking my mind off work whenever I visited home. Thank you to my Dad and my brother for being there when I needed them. Thank you to my grandparents Betty, Peter and Barclay for our long phone calls which were always able to cheer me. Also I would like to thank my granny Sally who I miss deeply. Most importantly I thank my Mum who is my rock and whose continued love and support humbles me almost every day. Without my families continued and unwavering support I would not have been able to reach this point. ii iii Abstract External space is mapped by a widespread brain circuit located in interconnected sub regions of the hippocampal-parahippocampal cortices. To date there have been 4 functionally specialised cell types identified providing information about location (place cells), heading direction (head direction cells), self-motion (grid cells) and boundaries (boundary vector cells and border cells). In the present thesis I present novel research identifying and characterising spatial cells located in the subiculum, an under explored region within the hippocampal formation. The subiculum is a key output structure from CA1 but also provides strong projections to the entorhinal cortex and pre- and parasubiculum, placing it ideally within the brain circuitry to contribute to the representations of external space. This thesis presents evidence for a variety of functionally and morphologically diverse spatial cells located in the subiculum. Critically I present the first ever report of subicular grid cells. These were recorded alongside boundary-responsive cells and head direction cells. The thesis characterises the basic properties of subicular grid cells, as tested in a variety of environmental manipulations. This thesis explores grid cell relationships to the environment and in particular to boundary manipulations. Among the key results in this thesis is the discovery that grid scale increases along the anterior- posterior axis of the subiculum, similar to MEC grid scale. This thesis also shows that subicular grid cell patterns can be disrupted with environmental manipulation. Wall removal caused grid patterns to shift orientation and increase grid scale. The grid scale expansion was related to novelty, which supports previous findings from MEC grid cells (Barry et al., 2007; 2012). This thesis also shows that grid patterns were disrupted by barrier insertion e.g. causing an inhibition to grid fields. When recorded in total darkness the grid cell patterns remained stable, suggesting that vision is not required for maintenance of the grid pattern structure. Taken together these findings provide evidence that grid cell firing patterns are at least partially determined by environmental boundaries. In addition this thesis extended upon the work of Lever et al., (2009), by presenting a detailed investigation and characterisation of subicular boundary vector cells (BVCs). I developed an empirical classification criterion, and utilised numerous manipulations to address the issue of what a BVC treats as a boundary. I also identified a new type of boundary related cell: the boundary-off cell. These cells have firing patterns which can be considered very similar to the iv inverse of the BVC. The inhibitory response of boundaries on these cells may provide a mechanism to explain the field inhibition seen in grid cells with barrier insertion. The data in this thesis presents novel research identifying and characterising spatial cells located in the subiculum. Of particular importance, is the discovery of grid cells in this structure that are intermingled with HD and boundary-responsive cells. The thesis focuses on characterising and investigating the importance of environment boundaries to subicular cell firing patterns. The results are discussed in relation to what is known about spatial representation in the hippocampal and parahippocampal regions, and the neural circuitry which comprises this representation. v Abbreviations AC Alternating current BVC Boundary vector cell CA Cornu ammonis Cm Centimetre COP Circular open platform DG Dentate Gyrus EC Entorhinal cortex EEG Electroencephalography HD Head direction Hz Hertz i.m. Intramuscular i.p . Intraperitoneal ITI inter trial interval Kg Kilograms LEC Lateral entorhinal cortex LED Light Emitting Diode LH Left hemisphere LWC Large walled circle LWS Large walled square M Metres MEC Medial entorhinal cortex µm Microns µs Microseconds µv Microvolts ml Millilitres ms Milliseconds RH right hemisphere s.c. Subcutaneous SE Standard error SEM Standard error of the mean SWS Small walled square vi Contents Abstract ............................................................................................................................................ iii Contents ........................................................................................................................................... vi Figure contents ........................................................................................................................... xiii Chapter 1 Introduction part 1: Anatomy of the hippocampal formation ...... 1 1.1 Nomenclature .......................................................................................................................... 1 1.2 Gross morphology ................................................................................................................
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