Behavioral correlates of human hippocampal delta and theta oscillations during navigation

Abstract

Previous rodent studies demonstrate movement-related increases in theta oscillations, and recent evidence suggests that multiple navigationally relevant variables are reflected in this activity. Human invasive recordings have revealed movement-related modulations in delta and theta activity, although it is unclear whether additional behavioral variables are responsible for modulating this neural activity during navigation. We tested the role of delta and theta oscillations during navigation by addressing whether spatial-related processing, in addition to speed and task variables, modulates delta and theta activity. Recording from 317 hippocampal intracranial electrodes in 10 patients undergoing seizure monitoring, we observed increasing delta and theta power with increasing virtual speed at significantly more electrodes than would be expected by chance, replicating previous findings in nonhuman mammals. Delta and theta power were more consistently modulated, however, as a function of spatial view, including when subjects looked at stores in the virtual environment both to find a relevant goal or for spatial updating. A significantly larger proportion of electrodes showed view-related effects than speed-related modulations. Although speed, task, and spatial view affected delta and theta activity, individual electrodes were most frequently modulated by only one variable, rather than a combination of variables. These electrodes likely sampled independent delta and theta generators, which reflected movement-related and allocentric processing, respectively. These results extend previous findings in nonhuman mammals and humans, expanding our knowledge of the role of human hippocampal low-frequency oscillations in navigation.