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Behavioral and Neural Effects of Reasoning Training by Allyson Mackey Doctor of Philosophy in Neuroscience University of California, Berkeley

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Behavioral and Neural Effects of Reasoning Training by Allyson Mackey Doctor of Philosophy in Neuroscience University of California, Berkeley Behavioral and Neural Effects of Reasoning Training by Allyson Mackey A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Neuroscience in the Graduate Division of the University of California, Berkeley Committee: Professor Silvia A. Bunge, Ph.D. (Chair) Professor Robert T. Knight, M.D. Professor Sonia J. Bishop, Ph.D. Professor Susan I. Stone, Ph.D. Fall 2012 Abstract Behavioral and Neural Effects of Reasoning Training by Allyson Mackey Doctor of Philosophy in Neuroscience University of California, Berkeley Professor Silvia A. Bunge, Ph.D., Chair My thesis research has focused broadly on how the environment shapes the structure and function of prefrontal cortex, for better or worse. I am interested in understanding in how experience-dependent plasticity can be harnessed to boost, or in some cases, remediate prefrontal function. I focused on training reasoning, the ability to solve novel problems, for two reasons: 1) reasoning is highly predictive of academic outcomes, and 2) reasoning was originally conceptualized as a fixed trait, and many people, both in science and in the general public, still believe that reasoning is set in stone. I conducted two studies, one in children and one in adults, to test the predictions that reasoning ability is malleable, and that repeated practice with reasoning problems strengthens connectivity within the frontoparietal network that supports high-level cognition. In my first study, children from low socioeconomic status backgrounds participated in 8 weeks of training with computerized and non-computerized games that targeted either reasoning ability or cognitive speed. Training led to dissociable behavioral outcomes: children in the reasoning training group improved substantially on a matrix reasoning test, while children in the speed training group improved specifically on a measure of cognitive speed. Reasoning gains corresponded to roughly 10 points in performance IQ. These results indicated that reasoning is modifiable by training in this population. In my second study, I capitalized on the fact that adults are taught reasoning skills by courses aimed at improving performance on the Law School Admissions Test (LSAT). I recruited young adults who were enrolled in an LSAT preparation course, and age- and IQ-matched controls intending to take the LSAT in the future. Magnetic resonance imaging (MRI) measures were collected for all subjects during two scanning sessions separated by 90 days. I first tested whether reasoning training altered functional connectivity at rest. I found strengthened fronto-parietal and parietal-striatal functional connectivity, particularly between hemispheres. I next investigated whether structural connectivity, as measured by diffusion in white matter, had been altered by training. I found training-related radial diffusivity (RD) decreases in white matter connecting frontal cortices, and mean diffusivity (MD) decreases closer to cortex in white matter in left frontal lobe and right parietal lobe. In conclusion, my thesis research has demonstrated that training can improve reasoning ability and, in adults, alter functional and structural connectivity. These results provide evidence for neural plasticity in large-scale networks supporting high-level cognition. 1 Dedication To my high school biology teacher, Richard Irwin, who encouraged me to think like a scientist, and to aspire to be one. i Acknowledgments Many people helped to make this work possible. Thank you, first, to my advisor and mentor, Silvia Bunge, and to the members of my committee, for helping me through this process. Thank you, too, to my friends and family who provided emotional and moral support along the way. Research Assistance Chapter 2: Thank you to Natalie DeShetler, Sasha Gupta, Rohan Oberoi, Monique Porsandeh, and Jeff Chu for supervising the training sessions, Kirstie Whitaker, Zdena Op de Macks and Ori Elis for their help with pre- and post- training assessments, Alejandro Ponce for his help with Spanish translation, and Emilio Ferrer and Carter Wendelken for comments on drafts of the manuscript. Chapters 3 and 4: Thank you to Chloe Green, Talia Seider, Sarah Inkelis, Brendan Berry, and Josh Hoerger for assistance with data collection. Thanks to Ariel Rokem, Elizabeth Mormino, Carter Wendelken, Matthew Brett, Jean- Baptiste Poline, Miles Lopes, and Andrew Conway for helpful discussions about data analysis. Co-author Contributions Chapter 2: A.P.M. designed the experiment, collected data, analyzed data, and wrote the paper. S.S.H. collected data. S.I.S. performed statistical analyses and commented on drafts. S.A.B. designed the experiment and wrote the paper Chapter 3: A.P.M. designed the experiment, collected data, analyzed data, and wrote the paper. A.M.S. collected data. S.A.B. designed the experiment and wrote the paper. Chapter 4: A.P.M. designed the experiment, collected data, analyzed data, and wrote the paper. K.J.W. designed data analyses and wrote the DTI methods. S.A.B. designed the experiment and wrote the paper. Funding My first year was supported by the Helen Wills Neuroscience Institute. My second year was supported by the T. O. Liu Fellowhip. My final three years were supported by a predoctoral fellowship from the National Science Foundation. Research presented in Chapter 2 was funded by the University of California at Berkeley and an R01 grant from the National Institute on Neurological Disorders and Stroke (NINDS)(NS057146-01). Research presented in Chapters 3 and 4 was funded by an NINDS Program Project grant (NS040813, Lead PI: D’Esposito, Co-Investigator: Bunge). ii Table of Contents Chapter 1 Introduction: Environmental Influences on Prefrontal Function.............................1 Modified from Mackey AP, Raizada RDS, and Bunge SA. Environmental Influences on Prefrontal Development. In Principles of Frontal Lobe Function, 2nd Edition, ed. Donald T. Stuss and Robert T. Knight. Oxford University Press, in press. Chapter 2 Reasoning training in children from low socioeconomic backgrounds.................16 Published as Mackey AP, Hill SS, Stone SI, and Bunge SA. Differential effects of reasoning and speed training in children. Dev Sci. 2011 May; 14(3): 582-590. Chapter 3 Reasoning training in adults alters brain connectivity at rest...............................30 Submitted as Mackey AP, Miller-Singley AT, and Bunge SA. Intensive reasoning training alters patterns of brain connectivity at rest. Chapter 4 Reasoning training in adults alters white matter microstructure..........................42 Submitted as Mackey AP, Whitaker KJ, and Bunge SA. Experience- dependent plasticity in white matter microstructure: Reasoning training alters frontoparietal connectivity. Chapter 5 Summary and future directions............................................................................57 References..........................................................................................................60 Appendices A. Supplemental material for chapter 2................................................................80 B. Supplemental material for chapter 3................................................................89 iii Chapter 1 Introduction: Environmental Influences on Prefrontal Development It takes only a few years for a human child’s sensory cortex to develop its full functionality. By contrast, it takes over two decades of experience and growth before prefrontal cortex (PFC) reaches its full maturity (Casey, Giedd, & Thomas, 2000; Fuster, 2002). A variety of studies have provided evidence that this prolonged period of development makes the PFC particularly sensitive to environmental influences – not only during the prenatal period and infancy, but also during childhood and adolescence (Andersen & Teicher, 2008; Crews, He, & Hodge, 2007). Among adults, as among children, there is a high degree of variability in cognitive functions that rely on PFC, including working memory (Vogel & Machizawa, 2004; Vogel, McCollough, & Machizawa, 2005) and cognitive control (Braver, Cole, & Yarkoni, 2010; Kane & Engle, 2002). Research on development and plasticity can provide important insights regarding the origins of individual differences in PFC-dependent cognitive functions. The focus of this chapter is on the role of the environment in shaping the development of the PFC – for better or for worse. There is substantial evidence that the development of prefrontal cortex can be hindered by a variety of environmental factors, including chronic stress as well as physical and psychosocial deprivation. However, there is also a growing body of research showing that various interventions could have a positive influence on brain function, or at least mitigate the effects of negative influences. This chapter provides an overview of research that provides evidence for both negative and positive environmental influences on prefrontal function, with an emphasis on prefrontal development. It then introduces the work in this thesis on improving reasoning ability, a prefrontal skill that has long been thought to be immutable to environmental influences. Negative environmental influences on prefrontal development Children who experience detrimental or simply insufficient environments encounter obstacles to reaching their full potential. Two crucial questions are how these obstacles can be prevented beforehand, and whether or how, once encountered, they can be overcome. Here, we consider in turn various negative influences on the development
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