Human cortical θ during free exploration encodes space and predicts subsequent memory.
Spatial representations and walking speed in rodents are consistently related to the phase, frequency, and/or amplitude of θ rhythms in hippocampal local field potentials. However, neuropsychological studies in humans have emphasized the importance of parietal cortex for spatial navigation, and efforts to identify the electrophysiological signs of spatial navigation in humans have been stymied by the difficulty of recording during free exploration of complex environments. We resolved the recording problem and experimentally probed brain activity of human participants who were fully ambulant. On each of 2 d, electroencephalography was synchronized with head and body movement in 13 subjects freely navigating an extended virtual environment containing numerous unique objects. θ phase and amplitude recorded over parietal cortex were consistent when subjects walked through a particular spatial separation at widely separated times. This spatial displacement θ autocorrelation (STAcc) was quantified and found to be significant from 2 to 8 Hz within the environment. Similar autocorrelation analyses performed on an electrooculographic channel, used to measure eye movements, showed no significant spatial autocorrelations, ruling out eye movements as the source of STAcc. Strikingly, the strength of an individual's STAcc maps from day 1 significantly predicted object location recall success on day 2. θ was also significantly correlated with walking speed; however, this correlation appeared unrelated to STAcc and did not predict memory performance. This is the first demonstration of memory-related, spatial maps in humans generated during active spatial exploration.
Institute for Neural Computation, University of California, San Diego, La Jolla, California 92093, Departments of Psychiatry and Human Behavior and Anatomy and Neurobiology, University of California, Irvine, Irvine, California 92697, Departments of Radiology, Neuroscience, and Psychiatry, University of California, San Diego, La Jolla, California 92093, and Program in Neurosciences, University of California, San Diego, La Jolla, California, 92093.
Joseph
J
Snider
Markus
M
Plank
Gary
G
Lynch
Eric
E
Halgren
Howard
H
Poizner
D000328:Adult; D000704:Analysis of Variance; D001931:Brain Mapping; D002540:Cerebral Cortex / Q000502:physiology*; D004569:Electroencephalography; D004576:Electromyography; D005106:Exploratory Behavior / Q000502:physiology*; D005133:Eye Movements; D005260:Female; D006801:Humans; D008297:Male; D008568:Memory / Q000502:physiology*; D009068:Movement / Q000502:physiology*; D011237:Predictive Value of Tests; D015203:Reproducibility of Results; D013028:Space Perception / Q000502:physiology*; D013826:Theta Rhythm / Q000502:physiology*; D014584:User-Computer Interface; D055815:Young Adult