The effects of acute stress on spatial navigation in men and women. by Dustin van Gerven BA ...

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The effects of acute stress on spatial navigation in men and women.

by

Dustin van Gerven
B.A., Vancouver Island University, 2010
M.Sc., University of Victoria, 2012

A Dissertation Submitted in Partial Fulfillment
of the Requirements for the Degree of

DOCTOR OF PHILOSOPHY

in the Department of Psychology

 Dustin van Gerven, 2016
University of Victoria

All rights reserved. This thesis may not be reproduced in whole or in part, by photocopy or other
means, without the permission of the author.
ii

Supervisory Committee

The effects of acute stress on spatial navigation in men and women.

by

Dustin van Gerven
B.A., Vancouver Island University, 2010
M.Sc., University of Victoria, 2012

Supervisory Committee

Dr. Ronald Skelton, Department of Psychology
Supervisor

Dr. Adam Krawitz, Department of Psychology
Departmental Member

Dr. Tony Robertson, Department of Psychology
Departmental Member

Dr. W. Jake Jacobs, University of Arizona, Department of Psychology
Outside Member
iii

Abstract
Supervisory Committee

Dr. Ronald Skelton, Department of Psychology
Supervisor

Dr. Adam Krawitz, Department of Psychology
Departmental Member

Dr. Tony Robertson, Department of Psychology
Departmental Member

Dr. W. Jake Jacobs, University of Arizona, Department of Psychology
Outside Member

Stress is known to impair spatial navigation in rat models of declarative memory, and
declarative memory in humans, but the effects on spatial navigation in humans are unclear. At
least four models have been proposed to account for the cognitive effects of stress, based on the
two different physiological stress response systems (the sympathetic-adrenal-medullary (SAM)
and the hypothalamic-pituitary-adrenal (HPA) systems) and the effects of these responses on the
hippocampus and (sometimes) other subcortical structures. In this dissertation, I examined the
effects of an acute (experimental) stressor on human spatial navigation in three variations of
virtual Morris water mazes designed to dissociate between hippocampus-dependent (allocentric)
and hippocampus-independent (egocentric) forms of navigation. Results were considered in the
light of all 4 models. Experiment 1 used a dual-strategy Morris water maze to test whether acute
stress influences navigational strategy selection and whether this effect is mediated by the
activation of the HPA or the SAM system. Surprisingly, stress increased hippocampus-based
strategy selection, and did so in the presence of SAM but not HPA activation. Experiment 2 used
new dual-strategy and place mazes to examine the effects of acute stress on both strategy
selection and allocentric navigational performance. It also attempted to contrast the effects of
stress at a short delay, which would favour mediation by the SAM system, and a longer, 30
minute delay (from stressor onset), which would favour mediation by the HPA system. Contrary
to expectations, results revealed no effect of stress when tested immediately and sex-dependent
impairments of performance (in females) and allocentric strategy selection (in males) at the delay.
Experiment 3 used the same mazes as Experiment 2, plus a new cue maze to examine the effects
of acute stress on strategy selection and both allocentric and egocentric navigational performance
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after a 30 minute delay. Results confirmed that stress reduces allocentric strategy selection and
impairs allocentric performance, but also has sex-dependent effects on egocentric performance:
in females, stress enhanced navigation (as expected) but in males, stress impaired it. None of the
4 models provided a good explanation for these results, suggesting that current accounts of the
cognitive effects of stress may be inadequate.
v

Table of Contents
Supervisory Committee .................................................................................................................. ii
Abstract .......................................................................................................................................... iii
Table of Contents ............................................................................................................................ v
List of Figures .............................................................................................................................. viii
List of Abbreviations ..................................................................................................................... ix
Acknowledgments........................................................................................................................... x
Dedication ..................................................................................................................................... xii
Chapter 1: Introduction ................................................................................................................... 1
Background ................................................................................................................................. 1
Stress. ...................................................................................................................................... 1
Effects of stress on cognition. ................................................................................................. 5
Understanding the effects of stress on spatial navigation. .................................................... 12
The role of Sex ...................................................................................................................... 26
The Present Research. ............................................................................................................... 27
Chapter 2: Experiment 1 ............................................................................................................... 29
Introduction ............................................................................................................................... 29
Background. .......................................................................................................................... 29
Summary of hypotheses: ....................................................................................................... 33
Method ...................................................................................................................................... 34
Participants. ........................................................................................................................... 34
Materials. .............................................................................................................................. 35
Procedure. ............................................................................................................................. 42
Data analysis. ........................................................................................................................ 46
Results ....................................................................................................................................... 47
Manipulation checks. ............................................................................................................ 47
Stress and navigational performance. ................................................................................... 51
Stress and navigational strategy selection. ............................................................................ 51
Navigation, HPA, and SAM axis activation. ........................................................................ 52
Discussion ................................................................................................................................. 53
Bridge to Experiment 2 ............................................................................................................. 60
Chapter 3: Experiment 2 ............................................................................................................... 61
Introduction ............................................................................................................................... 61
Background. .......................................................................................................................... 61
Key Issues. ............................................................................................................................ 66
Approach and hypotheses. .................................................................................................... 66
vi

Summary of hypotheses: ....................................................................................................... 68
Method ...................................................................................................................................... 69
Participants. ........................................................................................................................... 69
Materials. .............................................................................................................................. 69
Procedure. ............................................................................................................................. 76
Data analysis. ........................................................................................................................ 79
Results ....................................................................................................................................... 80
Manipulation checks. ............................................................................................................ 80
Stress and navigational strategy. ........................................................................................... 82
Stress and navigational performance. ................................................................................... 85
Navigation and SAM axis activation. ................................................................................... 88
Discussion ................................................................................................................................. 90
Bridge to Experiment 3 ............................................................................................................. 99
Chapter 4: Experiment 3 ............................................................................................................. 101
Introduction ............................................................................................................................. 101
Background. ........................................................................................................................ 101
Key Issues. .......................................................................................................................... 106
Approach and hypotheses. .................................................................................................. 106
Summary of hypotheses. ..................................................................................................... 109
Method .................................................................................................................................... 109
Participants. ......................................................................................................................... 109
Materials. ............................................................................................................................ 110
Procedure. ........................................................................................................................... 113
Data analysis. ...................................................................................................................... 116
Results ..................................................................................................................................... 117
Manipulation checks. .......................................................................................................... 117
Stress and navigational strategy. ......................................................................................... 120
Stress and allocentric performance. .................................................................................... 121
Stress and egocentric performance. .................................................................................... 123
Navigation and SAM axis activation. ................................................................................. 125
Discussion ............................................................................................................................... 128
Chapter 5: General Discussion.................................................................................................... 139
Overview ................................................................................................................................. 139
Dissertation rationale and review of main findings ................................................................ 139
Recap and logic of the 3 experiments. ................................................................................ 140
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Limitations .............................................................................................................................. 142
Discussion of the main issues and synthesis of the findings .................................................. 147
The effect of stress on human navigational strategy selection. .......................................... 147
The effect of stress on allocentric performance. ................................................................. 153
The effects of stress on egocentric performance. ................................................................ 155
Bringing together stress effects on strategy and performance. ........................................... 160
The relationship between navigation and the physiological correlates of stress. ............... 162
Reconciling the present results with the 4 models. ............................................................. 165
Other Considerations .............................................................................................................. 174
Cortical contributions to the effects of stress on navigation ............................................... 174
Stress, frontal cortex, top-down control, and navigation .................................................... 176
Stress, attention and navigation .......................................................................................... 177
Future Research ...................................................................................................................... 178
General Conclusion ................................................................................................................. 181
References ................................................................................................................................... 184
viii

List of Figures
Figure 1. The Modified Yerkes-Dodson model. .......................................................................... 15
Figure 2. The Temporal Dynamics model. .................................................................................. 17
Figure 3. The Hot/Cool Systems model. ...................................................................................... 21
Figure 4. The Uniform Shift model. ............................................................................................ 24
Figure 5. Experiment 1: A Standard trial in the Dual-Strategy maze. ......................................... 39
Figure 6. Experiment 1: Procedure. ............................................................................................. 43
Figure 7. Experiment 1: Time course of the PASAT effect on physiological measurements. .... 49
Figure 8. Experiment 1: The effect of the PASAT on SAM measures. ....................................... 50
Figure 9. Experiment 1. The effect of the PASAT on salivary cortisol. ...................................... 50
Figure 10. Experiment 1: The effect of the PASAT on navigational strategy selection. ............. 52
Figure 11. Sample starting views in the Dual-Strategy maze. ..................................................... 57
Figure 12. Comparison of original and updated Dual-Strategy maze starting views. ................. 64
Figure 13. Experiment 2: Standard trial views of the uDS maze. ................................................ 73
Figure 14. Experiment 2: Views of the Place maze. .................................................................... 75
Figure 15. Experiment 2: Procedure. ........................................................................................... 78
Figure 16. Experiment 2: Time course of the PASAT effect on physiological measurements. .. 81
Figure 17. Experiment 2: The effect of the PASAT on SAM measures. ..................................... 82
Figure 18. Experiment 2: Effect of PASAT stress on strategy selection. .................................... 83
Figure 19. Experiment 2: The effect of PASAT stress on immediate and delayed performance. 86
Figure 20. Experiment 3: Standard trial views of the Cue maze. .............................................. 112
Figure 21. Experiment 3: Procedure. ......................................................................................... 115
Figure 22. Experiment 3: Time course of the PASAT effect on physiological measurements. 118
Figure 23. Experiment 3: The effect of the PASAT on SAM measures. ................................... 119
Figure 24. Experiment 3: Effect of PASAT stress on strategy selection. .................................. 120
Figure 25. Experiment 3: The effect of PASAT stress on performance in the Place maze. ...... 122
Figure 26. Experiment 3: The effect of PASAT stress on performance in the Cue maze. ........ 124
Figure 27. Minimum Cue Error example. .................................................................................. 159
ix

List of Abbreviations
Theoretical Models
MYD Modified Yerkes-Dodson
TDM Temporal Dynamics Model
Stress Physiology
HPA Hypothalamic-Pituitary-Adrenal
SAM Sympathetic-Adrenal-Medullary
CRH Corticotropin-Releasing Hormone
MR Mineralocorticoid Receptor
GR Glucocorticoid Receptor
NE Norepinephrine
Stress Measurement
HR Heart Rate
BP Blood Pressure
SC Skin Conductance
CORT Cortisol
STAI State-Trait Anxiety Inventory
Stress Induction
PASAT Paced Auditory Serial Addition Task
TSST Trier Social Stress Task
Navigation Testing
MWM Morris Water Maze
uDS updated Dual-Strategy maze
ITP Inter-trial Probe
ITSP Inter-trial Strategy Probe
Other Testing
FAPA Farm Animals Paired Associates
IGT Iowa Gambling Task
x

Acknowledgments
I wish to express my heartfelt thanks to a number of people who helped make this
dissertation possible. Without a doubt, I would not have been able to complete this project
without the dedicated and insightful support of Dr. Ron Skelton. I have come to learn that a
supervisor who is willing to devote as much time and energy to a single graduate student as Dr.
Skelton has is extremely rare. He has provided hey support throughout every phase of this
project, and helped me overcome a number of difficult challenges. However, his influence on me
has extended well beyond this particular piece of work – under his supervision, I have learned a
great number of import skills that I will be able to employ in my career going forward. I am
extremely grateful for everything he has done for me.
My dissertation committee members have been extraordinarily valuable to me throughout
this work. I leaned heavily on the inspiration of Dr. Jacobs’ empirical and theoretical work on the
effects of acute stress and stress hormones on the brain throughout the development of this
research. He has provided valuable advice on my methodology as well. Dr. Tony Robertson has
been a huge support to me since I was an undergraduate student at Vancouver Island University.
Indeed, without Dr. Robertson, I may not have pursued graduate studies in Neuro/Bio
psychology at all. Finally, I owe much to Dr. Adam Krawitz, who graciously agreed to join my
committee, despite the fact that my research topic is somewhat distant from his own. Despite this,
he proved valuable advice on how to analyse my data.
I am also very grateful to Dr. Sonia Lupien. She is one of the world leaders in research on
the effects of stress on the brain, and her work served as an important foundation for the present
dissertation. I was humbled when she agreed to become my external examiner, and she has
provided excellent feedback that has greatly improved the thesis at the revision stage.