The functional role of human right hippocampal/parahippocampal theta rhythm in environmental encoding during virtual spatial navigation.
Low frequency theta band oscillations (4-8 Hz) are thought to provide a timing mechanism for hippocampal place cell firing and to mediate the formation of spatial memory. In rodents, hippocampal theta has been shown to play an important role in encoding a new environment during spatial navigation, but a similar functional role of hippocampal theta in humans has not been firmly established. To investigate this question, we recorded healthy participants' brain responses with a 160-channel whole-head MEG system as they performed two training sets of a virtual Morris water maze task. Environment layouts (except for platform locations) of the two sets were kept constant to measure theta activity during spatial learning in new and familiar environments. In line with previous findings, left hippocampal/parahippocampal theta showed more activation navigating to a hidden platform relative to random swimming. Consistent with our hypothesis, right hippocampal/parahippocampal theta was stronger during the first training set compared to the second one. Notably, theta in this region during the first training set correlated with spatial navigation performance across individuals in both training sets. These results strongly argue for the functional importance of right hippocampal theta in initial encoding of configural properties of an environment during spatial navigation. Our findings provide important evidence that right hippocampal/parahippocampal theta activity is associated with environmental encoding in the human brain. Hum Brain Mapp 38:1347-1361, 2017. © 2016 Wiley Periodicals, Inc.
ARC Centre of Excellence in Cognition and its Disorders, Macquarie University, Sydney, New South Wales, Australia.|Department of Cognitive Science, Macquarie University, Sydney, New South Wales, Australia.
Yi
Y
Pu
Brain and Psychological Sciences Research Centre, Swinburne University of Technology, Melbourne, Victoria, Australia.
Brian R
BR
Cornwell
Program in Neurosciences and Mental Health, Hospital for Sick Children Research Institute, Toronto, Ontario, Canada.|Institute of Medical Sciences and Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada.|Department of Medical Imaging, University of Toronto, Toronto, Ontario, Canada.
Douglas
D
Cheyne
ARC Centre of Excellence in Cognition and its Disorders, Macquarie University, Sydney, New South Wales, Australia.|Department of Cognitive Science, Macquarie University, Sydney, New South Wales, Australia.
Blake W
BW
Johnson
D000293:Adolescent; D000328:Adult; D000704:Analysis of Variance; D001931:Brain Mapping; D004569:Electroencephalography; D004777:Environment; D005260:Female; D007839:Functional Laterality / Q000502:physiology*; D006624:Hippocampus / Q000502:physiology*; D006801:Humans; D008279:Magnetic Resonance Imaging; D015225:Magnetoencephalography; D008297:Male; D018782:Maze Learning / Q000502:physiology; D020534:Parahippocampal Gyrus / Q000502:physiology*; D065854:Spatial Navigation / Q000502:physiology*; D013826:Theta Rhythm / Q000502:physiology*; D013997:Time Factors; D014584:User-Computer Interface; D055815:Young Adult
hippocampus; magnetoencephalography; spatial navigation; theta rhythm; virtual reality