NORTHWESTERN UNIVERSITY Validating Dissociations between Human Memory Subtypes: Conceptual Priming, Familiarity, and Recollection A DISSERTATION SUBMITTED TO THE GRADUATE SCHOOL IN PARTIAL FULFILLMENT OF THE REQUIREMENTS for the degree DOCTOR OF PHILOSOPHY Field of Neuroscience (Interdepartmental Neuroscience Program) By Joel Lawrence Voss EVANSTON, ILLINOIS June 2007 2 ABSTRACT Validating Dissociations between Human Memory Subtypes: Conceptual Priming, Familiarity, and Recollection Joel Lawrence Voss A comprehensive understanding of human memory requires both cognitive and neural descriptions of memory processes along with a conception of how memory processing drives behavioral responses and subjective experiences. Noninvasive neuroimaging techniques have greatly extended our understanding of the functional characteristics of human memory, and how neural events give rise to different memory subtypes. Nonetheless, a great deal of uncertainty has clouded distinctions between hypothesized explicit memory processes termed recollection and familiarity, and a hypothesized implicit memory process termed conceptual priming. In this thesis, I specify this problem via a thorough review of findings from one form of neuroimaging, the recording of event-related brain potentials, and then outline a theoretical stance to justify why delineating these forms of memory has been particularly difficult from a neural perspective. I then present data from four neuroimaging experiments that clarify the neural relationships between these three expressions of memory. These neuroimaging experiments all employ novel behavioral paradigms in which multiple behavioral measures of memory subtypes substantiate the patterns of neuroimaging data, thus allowing valid conclusions to be made regarding the correspondence between behaviorally-indicated memory subtypes and neural measures. Taken together, results from these experiments indicate (1) that conceptual priming and familiarity are distinct forms of memory that are unlikely to result from the same neural processing, and (2) that familiarity and recollection, although phenomenologically distinct, are not qualitatively different in their neural implementation as revealed by electrophysiology, and thus likely reflect varying levels of explicit memory rather than distinct retrieval processes. 3 Contents Part One: Introduction 6 1. Human Memory Subtypes 7 2. ERP Recording and Analysis 8 3. Quantifying ERPs 11 4. Advantages and Disadvantages of the ERP Technique 13 Part Two: A Review of ERP Findings 5. ERPs and Memory Encoding 16 6. The Dm Approach 16 7. Intracranial Dm Findings 21 8. ERPs and Memory Retrieval 22 9. ERP Correlates of Recollection and Source Memory 24 10. ERP Correlates of Post-Retrieval Processing 27 11. Difficulties Identifying ERP Correlates of “Pure” Familiarity 29 12. Using ERPs to Contrast Memory Subtypes 32 13. Perceptual Priming and Recognition Memory 33 14. Conceptual Priming 36 Part Three: Existing Evidence against a Unique ERP Signature of Familiarity 15. Familiarity and Conceptual Priming 38 16. Variables That Cannot Differentiate Familiarity from Conceptual Priming 43 17. Variables That Can Potentially Differentiate Familiarity from Conceptual Priming 50 18. Direct Tests That Have Failed to Validate FN400 Correlates of Familiarity 53 Part Four: ERP Correlates of Familiarity and Conceptual Priming for Famous Faces 19. Rationale 57 20. Methods 58 21. Results 63 22. Discussion 70 Part Five: fMRI Correlates of Familiarity and Conceptual Priming for Famous Faces 23. Rationale 74 24. Methods 74 25. Results 78 26. Discussion 81 Part Six: ERP Correlates of Familiarity and Conceptual Priming for Minimalist Visual Shapes 27. Rationale 85 28. Methods 85 29. Results 90 30. Discussion 98 4 Part Seven: ERP Correlates of Familiarity and Conceptual Priming for Words 31. Rationale 102 32. Methods 102 33. Results 105 34. Discussion 111 Part Eight: Concluding Remarks 115 Bibliography 124 Illustrations Tables 1. Memory Taxonomy 140 2. Summary of fMRI Activation Clusters for Famous Faces 141 3. Conceptual Priming for Squiggles 142 4. Recognition Performance for Uncommon Words 143 5. Conceptual Priming for Uncommon Words 144 6. ERP Formal Comparisons for Uncommon Word Recognition 145 Figures 1. Event-Related Brain Potentials 146 2. The Subsequent Memory Paradigm 148 3. Representative LPC Encoding Effects 149 4. Representative LPC Retrieval Effects 151 5. Representative Late Frontal Effects 152 6. Contrasting Recollection and Perceptual Priming 153 7. Paradigm Used to Examine ERPs to Famous Faces 154 8. ERP Correlates of Memory for Famous Faces 156 9. ERP Correlates of Familiarity for Famous Faces 158 10. Paradigm Used to Examine fMRI Responses to Famous Faces 159 11. fMRI Correlates of Memory for Famous Faces 160 12. fMRI Impulse Response Functions 162 13. Squiggle Stimuli 163 14. Recognition Performance for Squiggles 164 15. ERP Correlates of Recognition for Squiggles 165 16. ERP Correlates of Recollection and Familiarity for Squiggles 166 5 17. ERP Correlates of Conceptual Priming for Squiggles 167 18. Correlations between ERP and Behavioral Correlates of Recognition 168 19. Electrode Locations 169 20. ERP Correlates of Conceptual Priming for Uncommon Words 170 21. ERP Correlates of Recognition for Uncommon Words 171 Appendices 1. Biographical Cues 172 2. Uncommon Words 175 6 Part One: Introduction This thesis describes the use of noninvasive neuroimaging measures to probe the neural substrates of human memory. After outlining a taxonomy that has proven useful in characterizing various memory subtypes, I review the literature on event-related brain potential recordings and the insights they have provided with regard to substantiating distinctions within the taxonomy. I then highlight several border areas within this taxonomy that need further clarification: those between hypothesized memory processes known as recollection, familiarity, and conceptual priming. Comparisons between these forms of memory constitute the primary theoretical focus of this thesis, as described in Section 15. A literature review examining the difficulties associated with delineating these forms of memory follows. Finally, I present data from four neuroimaging experiments that make progress towards demarcating these boundaries, and suggest how further insights can be gained in this area. A portion of the sections herein derive from work that has been published previously, is currently under peer review, or is in preparation. The general review of electrophysiological studies of human memory presented in Part 1 and Part 2 contains information presented in (Voss & Paller, in press). Information presented in Part 3 echoes an argument presented in (Paller, Voss, & Boehm, in press). Part 4 describes an experiment presented in (Voss & Paller, 2006). Part 5 describes an experiment presented in (Voss, Reber, Mesulam, Parrish, & Paller, under review). Part 6 describes an experiment presented in (Voss & Paller, 2007). Part 7 describes an experiment presented in (Voss, Lucas, & Paller, in preparation). In presenting these findings here as a coherent whole, it is possible to identify theoretical links that otherwise remain elusive, and thus to clearly identify these experiments’ contributions to the understanding of human memory at-large. 7 1. Human Memory Subtypes Remembering is a multifaceted cognitive activity that can be partitioned into a set of component processes. These processes are sometimes interrelated and sometimes operate independently, and are expressed in different combinations under different circumstances. These distinct memory functions have been uncovered largely by studying the memory capabilities of both healthy individuals and patients with selective memory impairments, and can be assessed using different specialized memory tests. A variety of theoretical schemes have been used to categorize the memory phenomena measured in these tests, emphasizing either behavioral, cognitive/representational, neural, or subjective criteria (White, in press). Taxonomies of memory have guided research into fundamental questions about memory. However, a comprehensive understanding of memory must go beyond taxonomy by defining each component process in both cognitive and neural terms, by specifying the relationships between cognitive and neural descriptions, and by showing how neurocognitive processes produce memory behavior and associated conscious experiences. Amnesic patients have selective impairments in declarative memory, the ability to remember facts and events from the past, as assessed in recall and recognition tests. In contrast, other categories of memory phenomena, as listed in Table 1, are not impaired in amnesia (Grill- Spector, in press; Schacter, in press; Squire, in press). Expressions of declarative memory tend to coincide with the potential for making the metamemory judgment that memory is being expressed—the awareness of remembering. For these reasons, declarative memory is usually regarded as fundamentally distinct from other expressions of memory. Information can also be held in awareness for an extended period of time, while rehearsed and/or manipulated. Nonetheless, the emphasis here is on long-term memory 8 phenomena that take place when information that was initially encoded is later brought back to mind after a delay, which is what William James (1890, pp648) termed secondary memory. [For a current summary of research on primary memory or working memory, see D’Esposito (in press)] The neural substrates