Recollection and familiarity in rhesus monkeys (Macaca mulatta) Open Access

Basile, Benjamin Michael (2013)

Permanent URL: https://etd.library.emory.edu/concern/etds/g445cd88c?locale=en
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Abstract

Think of the last conference you attended. You likely had the common experience of seeing someone that looked very familiar, but were unable to remember their name or where you met them previously. This example illustrates the distinction between recollection, the ability to retrieve detailed information from memory, and familiarity, the vague sense that something you currently experience has been experienced previously. The distinction between recollection and familiarity is fundamental to theories of human memory, but is difficult to test in nonhuman animals. This dissertation collects three papers that describe attempts to characterize recollection and familiarity in a nonhuman primate species, rhesus monkeys (Macaca mulatta). Paper 1 provides evidence that monkeys can reproduce simple shapes from memory in a way that parallels the visual recall tests used with humans. Monkeys were more accurate at recognition than at recall, while remembering the same shapes under matched conditions, consistent with the theory that recall performance reflects recollection alone, whereas recognition performance reflects the combined effects of recollection and familiarity. Paper 2 provides evidence that recognition performance reflects two processes: quick familiarity and slow recollection. Recognition errors following quick responses were disproportionally false alarms to familiar but unstudied stimuli, and introducing a response deadline selectively increased false alarms. Paper 3 provides evidence that familiarity-based recognition is passive. A concurrent cognitive demand did not interfere with memory retention of items from a large image set, for which items can be identified as familiar or unfamiliar at test, but did impair retention of items from a small image set, for which familiarity at test was not useful and which likely required active working memory. Together, the findings from these studies represent a small step forward in our understanding of recollection and familiarity in monkeys.

Table of Contents

Table of contents

1. General introduction .....................................................................1

1.1. Recollection and familiarity in humans ......................................................2

1.2. Recollection and familiarity in nonhumans ................................................8

2. Introduction to Paper 1 .....................................................................................12

3. Paper 1: Monkeys recall and reproduce simple shapes from memory .......................................................................................13

3.1. Summary ...................................................................................................14

3.2. Results and discussion ..............................................................................15

3.3. Experimental procedures ..........................................................................25

3.3.1. Subjects and apparatus ....................................................................25

3.3.2. Initial training ..................................................................................26

3.3.3. Comparison with recognition ..........................................................26

3.3.4. Transfer of recall performance to novel shapes ..............................27

3.4. Acknowledgments .....................................................................................28

4. Introduction to Paper 2 ....................................................................................29

5. Paper 2: Recognition errors suggest fast familiarity and slow recollection in rhesus monkeys ...................................................30

5.1. Abstract ......................................................................................................31

5.2. Introduction ..............................................................................................32

5.3. Experiments 1a &1b ...................................................................................37

5.3.1. Results and discussion .....................................................................37

5.4. Experiment 2 ............................................................................................40

5.4.1. Results and discussion .....................................................................42

5.5. Experiment 3 .............................................................................................45

5.5.1. Results and discussion .....................................................................46

5.6. General discussion ....................................................................................48

5.7. Methods .....................................................................................................52

5.7.1. Experiments 1a & 1b ........................................................................52

5.7.1.1. Subjects and apparatus .........................................................52

5.7.1.2. Stimuli ...................................................................................53

5.7.1.3. Procedure ..............................................................................53

5.7.1.4. Data analysis .........................................................................54

5.7.2. Experiment 2 ....................................................................................54

5.7.2.1. Subjects and apparatus .........................................................54

5.7.2.2. Stimuli ...................................................................................55

5.7.2.3. Procedure ..............................................................................55

5.7.2.4. Data analysis .........................................................................56

5.7.3. Experiment 3 ....................................................................................56

5.7.3.1. Subjects and apparatus .........................................................56

5.7.3.2. Stimuli ...................................................................................56

5.7.3.3. Procedure ..............................................................................56

5.8. Acknowledgments .....................................................................................57

6. Introduction to Paper 3 ...................................................................................58

7. Paper 3: Dissociation of active working memory and passive recognition in rhesus monkeys ....................................................59

7.1. Abstract .....................................................................................................60

7.2. Introduction ..............................................................................................61

7.3. Experiment 1 .............................................................................................65

7.3.1. Methods ...........................................................................................66

7.3.1.1. Subjects and apparatus ........................................................66

7.3.1.2. Stimuli ...................................................................................66

7.3.1.3. Procedure ..............................................................................66

7.3.2. Results and discussion .....................................................................69

7.4. Experiment 2a-2c ......................................................................................71

7.4.1. Methods ............................................................................................71

7.4.1.1. Experiment 2a .......................................................................72

7.4.1.2. Experiment 2b ......................................................................72

7.4.1.3. Experiment 2c .......................................................................72

7.4.2. Results and discussion .....................................................................73

7.4.2.1. Experiment 2a .......................................................................73

7.4.2.2. Experiment 2b ......................................................................73

7.4.2.3. Experiment 2c .......................................................................74

7.5. General discussion ....................................................................................74

7.6. Acknowledgments .....................................................................................78

8. General discussion ......................................................................79

8.1. Conclusion ................................................................................................83

9. References ........................................................................................................85


List of Figures

General introduction

Figure 1. Schematic illustrating the distinction between recall and recognition tests of memory ...................................................4

Figure 2. Theoretical ROC curves from human recognition tests ........6

Paper 1: Monkeys recall and reproduce simple shapes from memory

Figure 1. Time course of a recall and recognition trial during comparison ............................................................................18

Figure 2. Comparison of recall and recognition accuracy as a function of delay ..................................................................................21

Figure 3. Recall performance on trained shapes and novel shapes during transfer tests .............................................................23

Paper 2: Recognition errors suggest fast familiarity and slow recollection in rhesus monkeys

Figure 1. False alarms and misses plotted as a function of response latency ...................................................................................39

Figure 2. Diagram of a match/non-match recognition test used in Experiment 2 .........................................................................41

Figure 3. False alarms and misses as a function of response time .....44

Figure 4. Error rates under normal and speeded responding .............47

Paper 3: Dissociation of active working memory and passive recognition in rhesus monkeys

Figure 1. Memory tests with four levels of concurrent cognitive demand .................................................................................68

Figure 2. Memory performance for familiar but not unfamiliar images is impaired by concurrent cognitive demand in a demand-dependent manner in monkeys ............................................70

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