The hallmark of spatial memory is the ability to link objects or landmarks with their spatial locations. Significant failures of spatial memory are among the first major clinical markers of neurodegenerative disease. The proposed research aims to illuminate the neural and cognitive mechanisms underlying human spatial memory through the analysis of electrocorticographic and single-neuron recordings taken as neurosurgical patients navigate through virtual environments in search of target objects or locations. The proposed studies will examine the relation between brain waves (oscillations), cellular responses, and subjects' behavior during several types of game-like virtual navigation tasks. Our first two aims focus on the coding of spatial information.
Aim 1 seeks to answer the question: How is the information necessary for (virtual) spatial navigation and spatial memory represented by neuronal activity in various brain regions? Aim 2 attempts to complement this knowledge by asking the question: How do these spatially-relevant neural systems code information? The third and fourth aims regard the spatial memory system as a dynamic entity, and investigate the ways in which the responses of this system change over time, due to learning and to modifications of the environment.
Aim 3 addresses the question of how spatial representations are acquired and transformed through experience.
Aim 4 investigates the interaction between spatial memory and verbal episodic memory. The research supporting this aim will enable us to link our research on spatial memory to the larger literature on the role of the medial-temporal-lobe system in declarative memory processes in humans and animals. The proposed studies are of direct relevance to the treatment of epilepsy, in which mapping of cognitive functions to brain regions during surgical procedures is crucial for ensuring good postsurgical outcome, as well as developing treatments for other disorders of memory and cognition.

Public Health Relevance

Humans and lower animals possess an amazing capacity to rapidly form long-lasting spatial representations and to flexibly utilize those representations for navigation and searching behavior. As cognitive scientists have developed increasingly sophisticated ideas about human spatial cognition, neurobiologists have uncovered a rich and detailed understanding of the neural basis of this skill in lower animals. The proposed work aims to bridge these two approaches by studying the neurophysiology of human spatial cognition. Through direct brain recordings that can be ethically obtained in neurosurgical patients, we aim to advance our understanding of the neural basis of human navigation and spatial memory and its relation to other key forms of memory.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Research Project (R01)
Project #
5R01MH061975-16
Application #
9441855
Study Section
Neurobiology of Learning and Memory Study Section (LAM)
Program Officer
Buhring, Bettina D
Project Start
2001-12-10
Project End
2020-01-31
Budget Start
2018-02-28
Budget End
2020-01-31
Support Year
16
Fiscal Year
2018
Total Cost
Indirect Cost
Name
University of Pennsylvania
Department
Psychology
Type
Schools of Arts and Sciences
DUNS #
042250712
City
Philadelphia
State
PA
Country
United States
Zip Code
19104
Lee, Sang Ah; Miller, Jonathan F; Watrous, Andrew J et al. (2018) Electrophysiological Signatures of Spatial Boundaries in the Human Subiculum. J Neurosci 38:3265-3272
Goyal, Abhinav; Miller, Jonathan; Watrous, Andrew J et al. (2018) Electrical Stimulation in Hippocampus and Entorhinal Cortex Impairs Spatial and Temporal Memory. J Neurosci 38:4471-4481
Maidenbaum, Shachar; Miller, Jonathan; Stein, Joel M et al. (2018) Grid-like hexadirectional modulation of human entorhinal theta oscillations. Proc Natl Acad Sci U S A 115:10798-10803
Herweg, Nora A; Kahana, Michael J (2018) Spatial Representations in the Human Brain. Front Hum Neurosci 12:297
Watrous, Andrew J; Miller, Jonathan; Qasim, Salman E et al. (2018) Phase-tuned neuronal firing encodes human contextual representations for navigational goals. Elife 7:
Haque, Rafi U; Wittig Jr, John H; Damera, Srikanth R et al. (2015) Cortical Low-Frequency Power and Progressive Phase Synchrony Precede Successful Memory Encoding. J Neurosci 35:13577-86
Greenberg, Jeffrey A; Burke, John F; Haque, Rafi et al. (2015) Decreases in theta and increases in high frequency activity underlie associative memory encoding. Neuroimage 114:257-63
Zhang, Honghui; Jacobs, Joshua (2015) Traveling Theta Waves in the Human Hippocampus. J Neurosci 35:12477-87
Miller, Jonathan F; Fried, Itzhak; Suthana, Nanthia et al. (2015) Repeating spatial activations in human entorhinal cortex. Curr Biol 25:1080-5
Burke, John F; Merkow, Maxwell B; Jacobs, Joshua et al. (2014) Brain computer interface to enhance episodic memory in human participants. Front Hum Neurosci 8:1055

Showing the most recent 10 out of 68 publications