Reset of human neocortical oscillations during a working memory task

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.

Fig. 1.

The Sternberg item recognition task. (a) Illustration of the experimental design. (b) Average activity recorded from a representative electrode. Onset of the orienting stimulus is denoted by the dotted vertical line, the four list items by the solid lines and the probe is denoted by the dashed line. Electrode located in the left inferior temporal lobe of participant 5. [Talairach coordinates: (L–R, A–P, I–S) = (-33, -56, -17) mm.]

Fig. 2.

Probes reset 8-Hz phase. (a) Filtered (6–10 Hz) single trials (blue lines) and average activity (red line) illustrating phase reset to the probes at the level of single trials for the 1-s interval surrounding probe onset (occuring at time t = 0). (b) An 8-Hz phase distribution 250 ms before the onset of the probe (calculated across 320 trials) is shown. (c) An 8-Hz phase distribution 250 ms after probe onset is shown. (d) Spectrogram showing average power (calculated across all trials, without filtering) at each frequency for the 1-s interval surrounding probe onset. For all panels, the electrode is the same as in Fig. 1b.

Fig. 3.

Patterns of phase reset across brain locations. (a) Phase-locking spectrogram illustrating degree of phase locking across frequency and time. The color scale represents the log₁₀ (P) value associated with the null hypothesis that the phase values (across trials) are uniformly distributed. Activity recorded from an electrode in right inferior temporal lobe in participant 9 [Talairach coordinates: (L–R, A–P, I–S) = (+14, -54, -3) mm]. Green bars denote the onset of the orienting stimulus, blue bars denote the onset of the list items, and red bars denote the onset of the probe stimulus. (b) Phase-locking spectrogram from an electrode in right subcallosal gyrus of participant 1 [Talairach coordinates: (L–R, A–P, I–S) = (+19, +1, -13) mm]. (c) Phase-locking spectrogram from a depth electrode in the right hippocampus of subject 4 [Talairach coordinates: (L-R, A-P, I-S) = (+25, -27, -19) mm]. (d) Phase-locking spectrogram from a depth electrode in the right occipital cortex of subject 7 [Talairach coordinates: (L–R, A–P, I–S) = (+39, -74, 3) mm]. (e) Phase-locking spectrogram from an electrode in the right inferior temporal lobe of subject 2 [Talairach coordinates: (L–R, A–P, I–S) = (+35, -39, -16) mm].

Fig. 4.

Phase reset is neither caused by item repetition nor accompanied by transient increases in power. (a) Number of electrodes exhibiting significant phase reset to the orienting stimulus (green), list items (blue), and probes (red) at each frequency. (b) Number of electrodes exhibiting significant phase reset to targets (blue) and lures (red). Conservative estimate of Type-I error rate is less than one electrode per frequency in both panels. (c) Correlation between postprobe power change and phase locking at each frequency. Asterisks denote significant correlations (P < 0.01).

Fig. 5.

Brain locations exhibiting preferential reset to each stimulus class. Topographic maps display the location of brain regions exhibiting preferential reset to each stimulus class. Red-, blue-, and green-filled shapes indicate preferential reset to the probe, list items, and the orienting stimulus, respectively. Unfilled shapes denote the 551 electrodes that were included in the analysis but did not exhibit preferential reset. Different shapes indicate different participants.