Entrainment of neural oscillations as a modifiable substrate of attention

Abstract

Brain operation is profoundly rhythmic. Oscillations of neural excitability shape sensory, motor, and cognitive processes. Intrinsic oscillations also entrain to external rhythms, allowing the brain to optimize the processing of predictable events such as speech. Moreover, selective attention to a particular rhythm in a complex environment entails entrainment of neural oscillations to its temporal structure. Entrainment appears to form one of the core mechanisms of selective attention, which is likely to be relevant to certain psychiatric disorders. Deficient entrainment has been found in schizophrenia and dyslexia and mounting evidence also suggests that it may be abnormal in attention-deficit/hyperactivity disorder (ADHD). Accordingly, we suggest that studying entrainment in selective-attention paradigms is likely to reveal mechanisms underlying deficits across multiple disorders.

Keywords: EEG; attention-deficit/hyperactivity disorder; dyslexia; entrainment; schizophrenia; selective attention.

Figure 1. Entrainment of neural oscillations

(a) Stylized example of oscillatory entrainment by rhythmic auditory stimuli. The excitability of neural ensembles oscillates at various frequencies. The phases of ongoing oscillations are reset by the first stimulus. The second stimulus establishes a rhythm, and oscillatory frequencies adjust such that phases become aligned to this rhythm. As a consequence of entrainment, neural ensembles are in a particular state of excitability when stimuli occur. Oscillations remain entrained for several cycles after the last stimulus before eventually “falling out of phase” due to frequency changes. (b) Supragranular current source density trace recorded from a monkey showing entrainment of ongoing oscillations to rhythmic auditory stimuli. Blue vertical lines represent stimuli and red lines represent when stimuli would have occurred if stimulation had continued. Oscillatory phase remained entrained to the stimulation rhythm for several cycles after the last stimulus (adapted, with permission, from [12]).

Figure 2. Hierarchical phase-amplitude coupling

Stylized example of phase-amplitude coupling in a hierarchy of oscillations. The top trace represents a typical EEG signal comprised of several oscillatory frequencies. The other three traces are the individual oscillations that are added to create the combined signal. The phase of lower frequency oscillations determines the amplitude of higher frequencies in a hierarchical fashion. The phase of the delta oscillation is coupled to the amplitude of the theta oscillation, such that theta amplitude is larger during one phase of delta and smaller during the opposite phase. The phase of the theta oscillation is similarly coupled to the amplitude of the gamma oscillation. Gamma oscillations are “co-modulated” by both delta and theta rhythms.

Figure 3. Entrained oscillatory phase affects perception

A recent study showing that the phase of entrained alpha oscillations affects stimulus detection (adapted, with permission, from [26]). (a) SOA = stimulus onset asynchrony, eSOA = entrainer SOA, tSOA = target SOA, mSOA = mask SOA. Participants were instructed to detect small circular targets that were backward-masked by an annulus. Each trial began with a fixation and blank screen, followed by an entraining period in which one of three conditions was presented. Eight annulus stimuli were presented with a fixed, 83 ms SOA (12 Hz) in the rhythmic condition and a variable SOA in the variable condition. The control condition presented only two annuli at the beginning and end of the entraining period. Targets were then presented at one of seven randomly chosen lags after the entraining period. Lags of 83 and 177 ms, indicated by blue boxes, were in-phase with the entrainment rhythm, meaning that they represented time points at which rhythmic stimuli would have occurred had entraining continued. Lags of 36 and 130 ms, indicated by pink boxes, were out-of-phase, meaning that they represented time points directly between rhythmic stimuli if entraining had continued. (b) Target detection as a function of target lag. In-phase targets (blue boxes) were detected more often than out-of-phase targets (pink boxes). For in-phase targets at 83 ms, detection rates were significantly higher for the rhythmic and variable conditions compared to the control condition. Detection rates were also significantly higher for the rhythmic than the variable condition. For in-phase targets at 177 ms, detection rates were also significantly higher for the rhythmic and variable conditions than the control condition, but the rhythmic and variable conditions did not differ. These results indicate that detection of targets was enhanced or suppressed during particular phases of the entrained oscillations. (c) Difference between phase-locking index (PLI) locked to onset of entrainment period for the rhythmic and variable conditions. PLI measures the consistency of a particular frequency’s phase at a given time across trials, reflecting phase alignment. The two marked time windows are 300 ms before and 200 ms after the end of entrainment, and the head plots show average scalp distributions of the PLI difference in these two windows. Initial fixation and entrainer stimuli are marked with vertical lines. This time-frequency plot shows increased PLI during entrainment for the rhythmic compared to the variable condition, centered on the 12 Hz entrainment frequency, coincident in time with the presentation of targets.

Figure 4. Oscillatory entrainment as a substrate of selective attention

(a) Stylized example of selective oscillatory entrainment. Rhythmic visual and auditory stimulus streams are presented simultaneously in anti-phase. Attention to the visual stream entrains ongoing oscillations such that a particular phase of the oscillation in neural excitability coincides with visual stimuli. Attention to the auditory stream, however, aligns that same phase to auditory stimuli, producing an oscillation pattern that is anti-phase to the visual attention condition. Under identical stimulus conditions, attention can determine the entrainment pattern by aligning particular states of neural excitability to one stream or another. (b) Intracranial recordings from epilepsy patients who performed a selective attention task. Interleaved visual and auditory streams were presented, and the task was to detect targets in one of the two modalities. The upper plots show the unfiltered EEG recordings time-locked to auditory or visual stimuli (time point 0). The two different colors represent EEG recordings under different attention conditions (visual vs. auditory). The lower plots show the same data filtered at the stimulus frequency (1.5 Hz). The oscillatory entrainment pattern is generally anti-phase between the two attention conditions, demonstrating selective entrainment to the attended stream (adapted, with permission, from [37]). We note the caveat that this effect may also be due to a general system for predicting stimuli, which happens to appear rhythmic under rhythmic stimulus conditions. Future work may differentiate between entrainment of ongoing oscillations and more general predictability mechanisms.