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. 2015 Jan 20:8:1055.
doi: 10.3389/fnhum.2014.01055. eCollection 2014.

Brain computer interface to enhance episodic memory in human participants

John F Burke  1 , Maxwell B Merkow  2 , Joshua Jacobs  3 , Michael J Kahana  4 , Kareem A Zaghloul  5
Affiliations

Brain computer interface to enhance episodic memory in human participants

John F Burke et al. Front Hum Neurosci. .

Abstract

Recent research has revealed that neural oscillations in the theta (4-8 Hz) and alpha (9-14 Hz) bands are predictive of future success in memory encoding. Because these signals occur before the presentation of an upcoming stimulus, they are considered stimulus-independent in that they correlate with enhanced memory encoding independent of the item being encoded. Thus, such stimulus-independent activity has important implications for the neural mechanisms underlying episodic memory as well as the development of cognitive neural prosthetics. Here, we developed a brain computer interface (BCI) to test the ability of such pre-stimulus activity to modulate subsequent memory encoding. We recorded intracranial electroencephalography (iEEG) in neurosurgical patients as they performed a free recall memory task, and detected iEEG theta and alpha oscillations that correlated with optimal memory encoding. We then used these detected oscillatory changes to trigger the presentation of items in the free recall task. We found that item presentation contingent upon the presence of pre-stimulus theta and alpha oscillations modulated memory performance in more sessions than expected by chance. Our results suggest that an electrophysiological signal may be causally linked to a specific behavioral condition, and contingent stimulus presentation has the potential to modulate human memory encoding.

Keywords: BCI; ECoG; episodic memory; theta.

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Figures

Figure 1
Figure 1
Brain computer interface free recall task: overview. Incoming ECoG data recorded by intracranial electrodes (A) was split and digitized by a Neuralynx recording system (B). The appropriate memory signal was decoded (C) in real-time (D) to control the memory experiment (E). The entire real-time loop (A–E) was performed within 50 ms.
Figure 2
Figure 2
Subsequent memory effect pre- and post-stimulus. (A) Across all patients, t-statistics (y-axis) comparing spectral power during the presentation of items that were later recalled vs. those that were later not-recalled are plotted for all frequencies (x-axis) for the post-stimulus interval (300–1500 ms after word onset). A positive t-statistic represents more power in the recalled vs. the not-recalled condition across all 14 patients. The yellow box marks the theta frequency range. The horizontal lines mark the p = 0.05 significance level. (B) The histogram displays the number of electrodes that showed a statistically reliable (p < 0.05) modulation of power during the post-stimulus interval. The horizontal line shows the number of electrodes that should be expected to be significant by chance at the p = 0.05 level. Panels (C,D) show identical plots for the pre-stimulus interval (0–1000 ms).
Figure 3
Figure 3
Example electrodes showing changes in theta during the pre-stimulus time interval. Panels (A,B) show example electrodes in two different patients that displayed marked modulations of theta power in the pre-stimulus interval during successful encoding. The electrodes were taken from the rostral mid-frontal region and the superior frontal region, respectively. The errorbars reflect standard errors on the mean, and the red and blue lines represent power during successful and unsuccessful encoding.
Figure 4
Figure 4
Post-hoc time-frequency analysis of spectral power during contingent conditions. The figure shows time-frequency power spectra averaged across all word presentations during the bciFR task. (A) In one participant, we selectively triggered word presentation on increases (left-panel) or decreases (right-panel) of an alpha oscillation. (B) In a second participant, we triggered word presentation on increases (left-panel) or decreases (right-panel) of a theta oscillation. Word presentation is indicated by the dashed line at t = 0. Color represent average z-scored power at every time point and every frequency for all word presentations during the contingent condition.
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