Reset of human neocortical oscillations during a working memory task

doi:10.1073/pnas.0732061100

Reset of human neocortical oscillations during a working memory task

^*Volen Center for Complex Systems, Brandeis University, Waltham, MA 02454; ^‡Department of Neurosurgery, Children's Hospital, Boston, MA 02115; ^§Department of Surgery, Harvard Medical School, Boston, MA 02115; ^¶Department of Neurology, Brigham and Women's Hospital, Boston, MA 02115; and ^∥Neurozentrum, Universitaet Freiburg, D-79106 Freiburg, Germany

Communicated by Saul Sternberg, University of Pennsylvania, Philadelphia, PA, April 8, 2003 (received for review May 22, 2002)

Abstract

Both amplitude and phase of rhythmic slow-wave electroencephalographic activity are physiological correlates of learning and memory in rodents. In humans, oscillatory amplitude has been shown to correlate with memory; however, the role of oscillatory phase in human memory is unknown. We recorded intracranial electroencephalogram from human cortical and hippocampal areas while subjects performed a short-term recognition memory task. On each trial, a series of four list items was presented followed by a memory probe. We found agreement across trials of the phase of oscillations in the 7- to 16-Hz range after randomly timed stimulus events, evidence that these events either caused a phase shift in the underlying oscillation or initiated a new oscillation. Phase locking in this frequency range was not generally associated with increased poststimulus power, suggesting that stimulus events reset the phase of ongoing oscillations. Different stimulus classes selectively modulated this phase reset effect, with topographically distinct sets of recording sites exhibiting preferential reset to either probe items or to list items. These findings implicate the reset of brain oscillations in human working memory.

Footnotes

↵ ** To whom correspondence should be addressed. E-mail: kahana{at}brandeis.edu.
↵ † Present address: Division of Biology, California Institute of Technology, Pasadena, CA 91125.
Abbreviations: EEG, electroencephalography; iEEG, intracranial EEG.
↵ †† This amount of jitter (150 ms) will fully randomize prestimulus phase for all frequencies above 6.6 Hz. At 4 Hz, the lowest frequency we consider, this amount of jitter will ensure that prestimulus phase is, at a minimum, uniformly distributed within a 270° arc (of a possible 360°). Analyses take temporal jitter into account by selecting epochs of iEEG that have been aligned to the stimulus in question. Because of the inclusion of temporal jitter, a given stimulus had a slightly different onset from trial to trial. Therefore, figures that show average activity across the entire trial (Figs. 1b and 3) utilize epochs of stimulus-aligned iEEG after each stimulus onset, concatenating them to illustrate the full time course of the trial. These figures thus contain a discontinuity at the time of stimulus onset.