Tuning of the human neocortex to the temporal dynamics of attended events

Abstract

Previous studies raise the hypothesis that attentional bias in the phase of neocortical excitability fluctuations (oscillations) represents a fundamental mechanism for tuning the brain to the temporal dynamics of task-relevant event patterns. To evaluate this hypothesis, we recorded intracranial electrocortical activity in human epilepsy patients while they performed an audiovisual stream selection task. Consistent with our hypothesis, (1) attentional modulation of oscillatory entrainment operates in a distinct network of areas including auditory, visual, posterior parietal, inferior motor, inferior frontal and superior midline frontal cortex, (2) the degree of oscillatory entrainment depends on the predictability of the stimulus stream, and (3) the attentional phase shift of entrained oscillation cooccurs with classical attentional effects observed on phase-locked evoked activity in sensory-specific areas but seems to operate on entrained low-frequency oscillations that cannot be explained by sensory activity evoked at the rate of stimulation. Thus, attentional entrainment appears to tune a network of brain areas to the temporal dynamics of behaviorally relevant event streams, contributing to its perceptual and behavioral selection.

Figure 1.

Location of significant 1.5 Hz entrainment and attentional phase shifts. Group maps of all the analyzed electrodes in all seven patients. The light gray electrodes did not show any effect, the dark gray electrodes showed an entrainment to the stimulation stream without an effect of attention, and the colored electrodes showed an effect of attention on the 1.5 Hz phase, either at the presentation the auditory stimulus (yellow), visual stimulus (blue), or both (green). Significant entrainments and effect of attention on the phase of the entrained rhythm were found in numerous brain areas. Data recorded at circled electrodes will be described in Figures 2 (red) and 3 (purple). Electrodes are displayed on a three-dimensional reconstruction of the cortical surface of the MNI single-subject structural MRI. Coordinates were normalized using the Talairach method and manually fitted based on stimulation mapping data and intraoperation photographs. X-coordinates of left hemisphere electrodes have been transformed to appear on the right hemisphere. Electrodes (except depth electrodes) are projected from a frame inside the hemisphere to the nearest surface vertex. The right bottom panel features a transparent cortical surface that allows one to see depth electrodes in the temporal/occipital cortex.

Figure 2.

Examples of 1.5 Hz entrainment and attentional 1.5 Hz phase shift. This figure displays the largest attentional phase opposition of the entrained 1.5 Hz rhythm for each patient (except for patient S5, who did not show attentional shift larger than π/2). The location of each electrode is identified on Figure 1. Phase opposition of the 1.5 Hz component between the attend auditory and attend visual conditions is sometimes readily visible in the unfiltered ECoG (A) but is evident in the 1.5 Hz-filtered signal (B). The histograms of 1.5 Hz phase values for both attentional conditions (C) show that this phase difference was present at the trial level. This effect is magnified by looking at the orientation of the mean phase vector across trials (D). All depicted phase-locking values were significantly different from zero and were significantly different between the attend auditory and attend visual conditions. Distribution of 1.5 Hz phase value across trials in different attentional conditions. The location of these six electrodes is indicated in Figure 1. Mean curves and phase distributions were locked either on auditory (blue) or visual (red) events. For more examples, see supplemental Figure 1 (available at www.jneurosci.org as supplemental material).

Figure 3.

Examples of different values of attentional phase shifts and phase-locking activity. This figure illustrates different values of attentional phase shifts for electrodes entrained to the stimulation stream. The first three columns illustrate electrodes showing a 1.5 Hz phase opposition between attend auditory and attend visual conditions (A–C). These electrodes showed no increase in PLV in frequencies >1.5 Hz after auditory (D, E) or visual (F, G) stimulation. The last two columns illustrate electrodes recording from the auditory and visual cortex, respectively. They both show a smaller (but significant) phase shift and important phase-locked activity after either auditory (D, E) or visual (F, G) stimulation, corresponding to large auditory and visual phase-locked activity (A). The locations of these five electrodes are shown in Figure 1. Note that all five electrodes show a significant PLV at 1.5 Hz, reflecting the significant 1.5 Hz entrainment that was the criterion for their inclusion in the phase difference analysis. The legends for rows A–C are the same as in Figure 2. PLVs are displayed between 0.7 and 60 Hz, between −1000 and 1000 ms. Only significant PLVs (not corrected) are displayed. The purple dashed frames indicate the time–frequency window in which the proportion of significant PLVs was measured for the correlation analysis (Fig. 4; supplemental Figs. 3, 4, available at www.jneurosci.org as supplemental material). For more examples, see supplemental Figure 2 (available at www.jneurosci.org as supplemental material).

Figure 4.

Correlation between the size of the attentional 1.5 Hz phase shift and the phase-locked 0.7–30 Hz activity. The size of the 1.5 Hz phase difference between attend auditory and attend visual conditions (A) was inversely proportional to the phase-locked activity in a 50–350 ms/0.7–30 Hz time–frequency window after stimulation (B). Note how the attentional phase shift is minimal and high-frequency phase-locked activity is maximal at electrodes recording from auditory and visual cortex. This inverse relationship is illustrated for each patient in C in a scatter plot form. Only electrodes with a significant (not corrected) phase shift are displayed. In B, we took the maximum values between auditory and visual trials. In C, each colored scatter plot and regression line corresponds to a different patient. The black line is the regression line for all points pooled together (correlation coefficient r = −0.50; p < 10⁻⁶).

Figure 5.

Density of significant effects across patients. a, The proportion of analyzed electrodes showing entrainment to the 1.5 Hz stimulus stream was higher in the precentral gyrus, the superior temporal gyrus (extending to the superior temporal sulcus), the angular gyrus, and the fusiform gyrus (colored areas). In contrast, the anterior frontal lobe and the anterior temporal lobe did not show a significant entrainment to the stimulus stream, despite extensive coverage (black areas). b, Among electrodes showing entrainment, the ventral motor cortex, the top of the superior temporal cortex, the angular gyrus, and the posterior fusiform gyrus showed a higher proportion of attentional phase shifts, whereas the inferior somatosensory cortex and inferior and posterior parts of the auditory cortex did not show any. In both panels, the hue/brightness scale (from black to red) codes for the density of electrodes with significant effect (either entrainment or attentional phase shift) and the saturation (from white to black/color) codes for the density of analyzed electrodes (in b, only electrodes showing entrainment in a were included). The maximum hue and saturation values were normalized to 1 separately for each map.

Figure 6.

Effect of regularity of the interstimulus interval on the size of the attentional phase shift. The size of the attentional phase shift was significantly larger when the ISI between sensory stimulation was regular and therefore the stimulation sequence predictable than when the ISI was randomly jittered. This histogram illustrates the increase in absolute phase shifts from the random to the regular ISI protocols, in two patients, at all the electrodes where the attentional phase shift was significant in both protocols. It is cumulated across the two patients. This increase was significant both at the patient level (patient S5: N = 7 electrodes; phase shift, 1.20 vs 0.66 rad; p < 0.05; patient S6: N = 52 electrodes; phase shift, 0.75 vs 0.56 rad; p < 10⁻³) and when data from both patients were pooled together (N = 59 electrodes; phase shift, 0.80 vs 0.57 rad; p < 10⁻⁴).