Neurocognitive networks in higher-level visual perception Mark A. Postans A Thesis submitted for the degree of Doctor of Philosophy (2015) Cardiff University School of Psychology Table of Contents Table of Contents ........................................................................................................ 1 Acknowledgements ..................................................................................................... 3 Chapter 1: Introduction............................................................................................... 4 1.1: Basic Anatomy of the EVC and MTL .................................................................. 6 1.2: The role of the EVC in visual perception .......................................................... 17 1.3: The MTL and declarative memory ................................................................... 23 1.4: Going beyond declarative memory in the MTL ................................................ 29 1.5: Representational accounts of memory and perception ................................... 46 1.6: Questions addressed by the current Thesis .................................................... 54 Chapter 2: Brain regions involved in perceptual processing for scenes, objects and faces .................................................................................................................... 63 2.1. Introduction ....................................................................................................... 63 2.2. Method .............................................................................................................. 69 2.3. Results .............................................................................................................. 78 2.4. Discussion......................................................................................................... 89 Chapter 3: White matter connections supporting perception for scenes, objects and faces .................................................................................................... 100 3.1. Introduction ..................................................................................................... 100 3.2. Method ............................................................................................................ 106 3.3. Results ............................................................................................................ 113 3.4. Discussion....................................................................................................... 124 Chapter 4: Dissociable roles for the fornix and inferior longitudinal fasciculus in discrimination accuracy for scenes and faces ............................................... 134 4.1. Introduction ..................................................................................................... 134 4.2. Methods .......................................................................................................... 139 4.3. Results ............................................................................................................ 143 4.4. Discussion....................................................................................................... 148 Chapter 5: Dissociable roles for the fornix and inferior longitudinal fasciculus in markers of perception for trial-unique scenes and faces .............................. 159 5.1 Introduction ...................................................................................................... 159 5.2. Method ............................................................................................................ 168 5.3. Results ............................................................................................................ 174 1 5.4. Discussion....................................................................................................... 180 Chapter 6: General Discussion .............................................................................. 192 6.1. Summary of findings ....................................................................................... 192 6.2 General conclusions ........................................................................................ 199 6.3. Limitations of the current work ....................................................................... 201 6.4. Outstanding questions .................................................................................... 205 6.5. Concluding remarks ........................................................................................ 209 References ............................................................................................................... 211 Appendix A –Tract-Based Spatial Statistics (TBSS) Analyses .......................... 237 2 Acknowledgements I’d like to begin by thanking my supervisor, Professor Kim Graham. I will always be grateful to Kim for taking a chance with me and giving me the opportunity to work in this fascinating field of academia. I think that Kim knows of my admiration for her so to spare her any potential embarrassment, I’ll just say here that it has been a privilege! I would also like to thank my colleagues within the Graham/Lawrence lab groups – Dr Hodgetts, Dr Umla-Runge, and Dr Muhlert in particular - for the friendship and professional support that they have extended to me throughout the duration of my PhD. I also owe my thanks to my colleagues at CUBRIC for all of the technical assistance that they have provided. I am especially grateful to Greg Parker who provided the Matlab code that was used to correct diffusion MR images for free water contamination in Chapters 3-5. I would also like to thank Dr Mariam Aly at the Princeton Neuroscience Institute for being generous with her advice on how to analyse perception receiver operating characteristics. On a more personal level, I am deeply grateful to my girlfriend Samantha for supporting my academic ambitions for what has been a protracted period of time. I know that it has been difficult at times but I can at least promise that I will not undertake another PhD! Finally, I could not have pursued my interests and ambitions without the support of my family. All of the things that my parents have done for me have not gone unnoticed and I hope to continue to make them proud. The same goes for the various matriarchs/patriarchs of our family: Barbara, Evelyn, Ralph and Sidney. 3 Chapter 1 Chapter 1: Introduction The ability to accurately perceive and respond to our visual environment is critical for optimising primate behaviour. A number of related cognitive functions, such as visual learning and longer-term memory, also depend upon an accurate percept of objects and their location within the visual environment. Understanding how the healthy brain supports higher-order visual perception is, therefore, a key goal for cognitive neuroscientists. A substantial body of research involving both humans and nonhuman primates has consistently demonstrated a role for regions within the extrastriate visual cortex (EVC) in visual perception, with many of these regions apparently exhibiting a high degree of functional specialisation for the processing of particular categories of complex stimuli (e.g. faces versus scenes). More recently, studies have also found that patients with selective damage to structures within the medial temporal lobe (MTL), such as the hippocampus (HC) and perirhinal cortex (PRC), present with not only the significant memory impairments associated with MTL amnesia (Squire et al., 2004), but also with category-sensitive impairments in visual perception, which seem to underpin category-sensitive deficits in visual memory. More specifically, damage to the PRC has been linked to impairments in perception for complex object-like stimuli such as faces, whereas HC damage has been linked to impairments in perception for visual scenes (Lee et al., 2005a). Such research has produced important insights into how multiple regions distributed across both the EVC and the MTL may make individual category- sensitive contributions to visual perception, but it remains unclear how these spatially distinct brain regions interact with one another, and to what extent their ability to interact underpins successful visual perception in humans. These issues are addressed here via a series of novel experiments involving the use of a combination of behavioural paradigms and magnetic resonance imaging (MRI) techniques in healthy human participants. These experiments aim to: a) investigate the distinct patterns of functional and structural connections that support the category- sensitive contributions of the PRC and HC to higher-level visual perception, and b) demonstrate that inter-individual variation in the structural properties of white matter pathways providing inputs/outputs to the PRC or HC is an important factor underpinning the contributions of these MTL regions to successful higher-level perception. These experiments are summarised briefly at the end of this Chapter, and are described in detail in Chapters 2-5. In Chapter 6, the findings of these experiments will be discussed in the context of representational accounts of perception, which, 4 Chapter 1 briefly, propose that multiple regions throughout the EVC and MTL construct and store perceptual representations of complex visual stimuli, and that the nature of the functional specialisation that exists across these regions is best described in terms of the type of representations