Anchoring The Cognitive Map To The Visual World

142 Pages·2017·11.04 MB·English

by  Joshua Benjamin Julian

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Publicly Accessible Penn Dissertations
2017
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Joshua Benjamin Julian
University of Pennsylvania, [email protected]
Follow this and additional works at: https://repository.upenn.edu/edissertations
Part of the Neuroscience and Neurobiology Commons
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Julian, Joshua Benjamin, "Anchoring The Cognitive Map To The Visual World" (2017). Publicly Accessible
Penn Dissertations. 2376.
https://repository.upenn.edu/edissertations/2376
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For more information, please contact [email protected].
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To interact rapidly and effectively with the environment, the mammalian brain needs a representation of
the spatial layout of the external world (or a “cognitive map”). A person might need to know where she is
standing to find her way home, for instance, or might need to know where she is looking to reach for her
out-of-sight keys. For many behaviors, however, simply possessing a map is not enough; in order for a
map to be useful in a dynamic world, it must be anchored to stable environmental cues. The goal of the
present research is to address this spatial anchoring problem in two different domains: navigation and
vision. In the first part of the thesis, which comprises Chapters 1-3, we examine how navigators use
perceptual information to re-anchor their cognitive map after becoming lost, a process known as spatial
reorientation. Using a novel behavioral paradigm with rodents, in Chapter 2 we show that the cognitive
map is reoriented by dissociable inputs for identifying where one is and recovering which way one is
facing. The findings presented in Chapter 2 also highlight the importance of environmental boundaries,
such as the walls of a room, for anchoring the cognitive map. We thus predicted that there might exist a
brain region that is selectively involved in boundary perception during navigation. Accordingly, in Chapter
3, we combine transcranial magnetic stimulation and virtual-reality navigation to reveal the existence of
such a boundary perception region in humans. In the second part of this thesis, Chapter 4, we explore
whether the same mechanisms that support the cognitive map of navigational space also mediate a map
of visual space (i.e., where one is looking). Using functional magnetic resonance imaging and eye
tracking, we show that human entorhinal cortex supports a map-like representation of visual space that
obeys the same principles of boundary-anchoring previously observed in rodent maps of navigational
space. Together, this research elucidates how mental maps are anchored to the world, thus allowing the
mammalian brain to form durable spatial representations across body and eye movements.
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Dissertation
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Doctor of Philosophy (PhD)
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Psychology
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Russell A. Epstein
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Neuroscience and Neurobiology
This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/2376
ANCHORING THE COGNITIVE MAP TO THE VISUAL WORLD
Joshua B Julian
A DISSERTATION
in
Psychology
Presented to the Faculties of the University of Pennsylvania
in
Partial Fulfillment of the Requirements for the
Degree of Doctor of Philosophy
2017

Supervisor of Dissertation
_________________________
Russell A. Epstein
Professor, Psychology

Graduate Group Chairperson
_________________________
Sara Jaffee
Professor, Psychology

Dissertation Committee
Geoffrey K. Aguirre, Assistant Professor, Neurology
Dan D. Lee, Professor, Electrical and Systems Engineering
Joshua Jacobs, Assistant Professor, Biomedical Engineering
Michael J. Kahana, Professor, Psychology
ANCHORING THE COGNITIVE MAP TO THE VISUAL WORLD
COPYRIGHT
2017
Joshua B. Julian

This work is licensed under the
Creative Commons Attribution-
NonCommercial-ShareAlike 3.0
License

To view a copy of this license, visit
https://creativecommons.org/licenses/by-nc-sa/3.0/us/
Dedicated to Laura

iii
ACKNOWLEDGMENT

I am extremely grateful to a number of people who made this dissertation possible.
First, thank you to my graduate advisor, Russell Epstein. Russell has been a constant
source of wisdom, support, and instructive feedback. Beyond inspiring me with his infectious
enthusiasm for science, Russell provided me with a model of what it means to be a good
scientist, and for that I am forever grateful. Thank you also to other members of my dissertation
committee—Geoff Aguirre, Dan Lee, Mike Kahana, and Josh Jacobs—for their insightful
comments and criticisms.
Second, I feel extremely lucky to have had a number of other brilliant mentors and
collaborators over the course of my graduate career. Thank you to Alex Keinath, frequent
collaborator and co-author—I cannot imagine a more productive collaboration, and certainly not
one that is more fun. Thank you to Jack Ryan, for help with the work presented here in Chapter 3
among other research, and Giulia Frazzetta, collaborator on the work presented here in Chapter
4. Thank you to all the talented, hard-working research assistants I have had over the course of
my graduate career: Sara Diaz, Monica Osher, Peter Bryan, and Rachel Freilich. Thank you to
the other members of the Epstein Lab family for creating a scientific environment that was
simultaneously interesting, challenging, and outrageously fun. Thank you also to the great
teachers and mentors with whom I have had the honor to learn from and work alongside: Isabel
Muzzio, Roy Hamilton, Danny Dilks, Nancy Kanwisher, and David Brainard.
Finally, thank you to my family their unconditional support of all of my endeavors,
academically and beyond. I especially thank my partner, Laura, for everything. Suffice it to say,
without Laura many of my cognitive maps would be unmoored and I would certainly feel lost.

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ABSTRACT

ANCHORING THE COGNITIVE MAP TO THE VISUAL WORLD
Joshua B. Julian
Russell A. Epstein

To interact rapidly and effectively with the environment, the mammalian brain needs a
representation of the spatial layout of the external world (or a “cognitive map”). A person might
need to know where she is standing to find her way home, for instance, or might need to know
where she is looking to reach for her out-of-sight keys. For many behaviors, however, simply
possessing a map is not enough; in order for a map to be useful in a dynamic world, it must be
anchored to stable environmental cues. The goal of the present research is to address this spatial
anchoring problem in two different domains: navigation and vision. In the first part of the thesis,
which comprises Chapters 1-3, we examine how navigators use perceptual information to re-
anchor their cognitive map after becoming lost, a process known as spatial reorientation. Using a
novel behavioral paradigm with rodents, in Chapter 2 we show that the cognitive map is
reoriented by dissociable inputs for identifying where one is and recovering which way one is
facing. The findings presented in Chapter 2 also highlight the importance of environmental
boundaries, such as the walls of a room, for anchoring the cognitive map. We thus predicted that
there might exist a brain region that is selectively involved in boundary perception during
navigation. Accordingly, in Chapter 3, we combine transcranial magnetic stimulation and virtual-
reality navigation to reveal the existence of such a boundary perception region in humans. In the
second part of this thesis, Chapter 4, we explore whether the same mechanisms that support the
cognitive map of navigational space also mediate a map of visual space (i.e., where one is
looking). Using functional magnetic resonance imaging and eye tracking, we show that human
entorhinal cortex supports a map-like representation of visual space that obeys the same
principles of boundary-anchoring previously observed in rodent maps of navigational space.
v
Together, this research elucidates how mental maps are anchored to the world, thus allowing the
mammalian brain to form durable spatial representations across body and eye movements.
vi
TABLE OF CONTENTS
ABSTRACT.....................................................................................................................................v
LIST OF TABLES..........................................................................................................................viii
LIST OF ILLUSTRATIONS.............................................................................................................ix
PREFACE.......................................................................................................................................x
CHAPTER 1. The cognitive and neural basis of spatial reorientation.............................................1
1.1 Theoretical considerations: What is reorientation?...............................................................1
1.2 Cognitive Mechanisms of Reorientation................................................................................3
1.3 Neural Mechanisms for Reorientation...................................................................................9
1.4 Where do the perceptual inputs come from?......................................................................16
1.5 Conclusions.........................................................................................................................22
CHAPTER 2: Context recognition and heading retrieval are mediated by dissociable cognitive
systems in mice.............................................................................................................................29
2.1 Abstract...................................................................................................................................29
2.2 Introduction.........................................................................................................................30
2.3 Results................................................................................................................................32
2.4 Discussion...........................................................................................................................36
2.5 Methods..............................................................................................................................41
CHAPTER 3: The Occipital Place Area is causally involved in representing environmental
boundaries during navigation........................................................................................................49
3.1 Abstract...............................................................................................................................49
3.3 Discussion...........................................................................................................................55
3.3 Methods..............................................................................................................................57
CHAPTER 4: Human entorhinal cortex represents visual space using a boundary-anchored grid
......................................................................................................................................................70
4.1 Abstract...............................................................................................................................70
4.2 Results and discussion.......................................................................................................71
4.2 Methods..............................................................................................................................74
POSTFACE...................................................................................................................................89
APPENDIX....................................................................................................................................94
BIBLIOGRAPHY.........................................................................................................................108

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LIST OF TABLES

Table 3.1 Complete results of the analyses of variance performed on data from blocks 2-3
of Experiment 1
Table 3.2 Complete results of the analyses of variance performed on performance data from
blocks 2-3 of Experiment 2

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