SHORTCUTS FOR FEAR IN HIERARCHICAL VISUAL SYSTEMS Jessica McFadyen Bachelor of Psychological Science (Hons I) A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2018 Queensland Brain Institute ABSTRACT It is crucial to our survival that we can rapidly predict, detect, and respond to potential threats in our environment. As highly visual creatures, we have developed sophisticated neural networks for processing visual information about the world around us. Both the visual system and the amygdala are arguably the most thoroughly studied components of the brain and yet there is considerable controversy over how these two systems interact to rapidly respond to signs of threat. The work presented in this thesis aimed to resolve this controversy by investigating the structural and effective neural connectivity underlying rapid responses to fearful faces, with a particular focus on a pathway from the superior colliculus to the amygdala via the pulvinar that bypasses the visual cortex. This thesis also aimed to extend our understanding of how neural shortcuts for fear may influence the overall, hierarchical structure of the human brain, particularly regarding its ability to predict and to produce our conscious visual experience. In Chapter 2, I used a combination of magnetoencephalography (MEG) and dynamic causal modelling (DCM) to show that a subcortical connection between the pulvinar and the amygdala rapidly conveys both coarse (i.e. low spatial frequencies) and fine (i.e. high spatial frequencies) visual information about neutral and fearful faces. These results offer new evidence for a rapid but functionally-indistinct pulvino-amygdala connection that may receive multiple sources of input from early visual areas. In Chapter 3, I investigated how the structural connectivity between subcortical visual areas and the amygdala relates to neural activity and behaviour evoked during face perception. I reconstructed white matter fibres from the superior colliculus, the pulvinar, and the amygdala, using diffusion-weighted images (DWI) from over 600 participants. For the pulvino-amygdala connection, greater fibre density correlated with stronger functional coupling (as given by dynamic causal modelling for fMRI) during face perception, as well as more accurate fearful face recognition. These novel relationships between anatomy and function provide unparalleled evidence for a subcortical pulvino-amygdala connection involved in fearful face processing. Finally, in Chapter 4, I investigated whether our conscious perception of faces differs depending on our prior expectations for threat. I discovered that prior expectations accelerate conscious access to neutral but not fearful faces, which were the most consciously-accessible stimuli overall (Experiment 1), especially when unexpected (Experiment 2). Model-based electroencephalography (EEG) analysis revealed that prior expectations hasten stimulus encoding in the visual cortex, while surprising fearful faces elicit accelerated evidence accumulation in the right inferior frontal gyrus. This newly discovered influence of aversive prediction errors on conscious perception has strong implications for how emotion and prediction networks interact in the brain. In conclusion, this thesis significantly furthers our understanding of how visual processing rapidly interacts with the amygdala to facilitate fearful face processing. Furthermore, these findings open up a new area of investigation into how the predictive brain operates under threat. i DECLARATION BY AUTHOR This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis. ii PUBLICATIONS DURING CANDIDATURE PEER-REVIEWED PAPERS *McFadyen, J, Mattingley, JB, Garrido, MI (accepted) An afferent subcortical white matter pathway to the amygdala facilitates fear recognition. eLife Baumann O, Vromen, JM, Cheung, A, McFadyen, J, Ren, Y, Guo, CC. (2018) Neural correlates of temporal complexity and synchrony during audiovisual correspondence detection. eNeuro, 5:0294. Bret, A, Beffara, B, McFadyen, J, Mermillod, M (2017) Right wing authoritarianism is associated with race bias in face detection. PloS one, 12:e0179894. *McFadyen, J, Mermillod, M, Mattingley, JB, Halász, V, Garrido, MI (2017) A rapid subcortical amygdala route for faces irrespective of spatial frequency and emotion. J Neurosci, 37:3864-3874. Bednark, JG, Poonian, SK, Palghat, K, McFadyen, J, Cunnington, R (2015) Identity-specific predictions and implicit measures of agency. Psychology of Consciousness: Theory, Research, and Practice, 2:253. Cao, Y, Contreras-Huerta, LS, McFadyen, J, Cunnington, R (2015) Racial bias in neural response to others' pain is reduced with other-race contact. Cortex, 70:68-78. Poonian, SK, McFadyen, J, Ogden, J, Cunnington, R (2015) Implicit agency in observed actions: evidence for N1 suppression of tones caused by self-made and observed actions. J Cog Neurosci, 27:752-764. IN PREPARATION *McFadyen J, Tsuchiya, N, Mattingley, JB, Smout, C, Garrido MI (in prep.) Expectations speed up conscious perception of neutral but not fearful faces CONFERENCE ABSTRACTS McFadyen, J, Taylor, JA, Smout, C, Mattingley, JB, Tsuchiya, N, Garrido, MI (2018) “The influence of neural activity and prior expectations on emotional breakthrough into conscious awareness” Oral presentation at Association for the Scientific Study of Consciousness (ASSC) Conference, Krakow, Poland McFadyen, J, Mattingley, JB, Garrido, MI (2017) “Fibre density of the subcortical route to the amygdala enhances fearful face perception: Converging evidence from tractography and DCM in the HCP dataset” Poster at Systems and Computational Neuroscience Down Under (SCiNDU), Brisbane, Australia McFadyen, J, Mattingley, JB, Garrido, MI (2017) “Fibre density of the subcortical route to the amygdala enhances fearful face perception: Converging evidence from tractography and DCM in the HCP dataset” Poster at International Cognitive Neuroscience Society Conference (ICON), Amsterdam, The Netherlands iii McFadyen, J, Mattingley, JB, Garrido, MI (2016) “Dynamic functional architectures of the human brain.” Invited symposium speaker at Australasian Cognitive Neuroscience Society (ACNS) Conference, Shoal Bay, Australia McFadyen, J, Lord, A., & Garrido, MI (2016) “Mapping the structure and function of the subcortical route to the amygdala in 600 subjects” Poster at NeuroEng: The Australasian Workshop on Neuro-Engineering and Computational Neuroscience, Brisbane, Australia McFadyen, J, Au, T, Copland, D, Dissanayaka, N. (2016) “The neuromodulatory role of anxiety in Parkinson’s Disease: An affective priming EEG study.” Poster at Royal Brisbane Women’s Hospital Symposium, Brisbane, Australia McFadyen, J, Mermillod, M, Mattingley, JB, Halász, V, Garrido, MI (2016) “Structural and effective amygdala pathways involved in spatial frequency and emotion processing.” Poster at Organisation for Human Brain Mapping (OHBM), Geneva, Switzerland McFadyen, J, Mermillod, M, Mattingley, JB, Halász, V, Garrido, MI (2015) “The subcortical route to the amygdala: spatial frequencies and facial expressions.” Poster at Systems and Computational Neuroscience Down Under (SCiNDU), Brisbane, Australia McFadyen, J, Mermillod, M, Mattingley, JB, Halász, V, Garrido, MI (2015) “The subcortical route to the amygdala: spatial frequencies and facial expressions” Oral presentation at Australasian Cognitive Neuroscience Society (ACNS) Conference, Auckland, New Zealand * Publication included in this thesis iv PUBLICATIONS INCLUDED IN THIS THESIS Incorporated as Chapter 2: McFadyen, J, Mermillod, M, Mattingley, JB, Halász, V, Garrido, MI (2017) A rapid subcortical amygdala route for faces irrespective of spatial frequency and emotion. J Neurosci, 37:3864-3874. Contributor Statement of Contribution Designed experiment (10%) Wrote paper (100%) Jessica McFadyen Collected data (50%) Edited paper (60%) Analysed data (85%) Martial Mermillod Designed