Attention Reorients Periodically

Abstract

Reorienting of voluntary attention enables the processing of stimuli at previously unattended locations. Although studies have identified a ventral fronto-parietal network underlying attention [1, 2], little is known about whether and how early visual areas are involved in involuntary [3, 4] and even less in voluntary [5] reorienting, and their temporal dynamics are unknown. We used transcranial magnetic stimulation (TMS) over the occipital cortex to interfere with attentional reorienting and study its role and temporal dynamics in this process. Human observers performed an orientation discrimination task, with either valid or invalid attention cueing, across a range of stimulus contrasts. Valid cueing induced a behavioral response gain increase, higher asymptotic performance for attended than unattended locations. During subsequent TMS sessions, observers performed the same task, with high stimulus contrast. Based on phosphene mapping, TMS double pulses were applied at one of various delays to a consistent brain location in retinotopic areas (V1/V2), corresponding to the evoked signal of the target or distractor, in a valid or invalid trial. Thus, the stimulation was identical for the four experimental conditions (valid/invalid cue condition × target/distractor-stimulated). TMS modulation of the target and distractor were both periodic (5 Hz, theta) and out of phase with respect to each other in invalid trials only, when attention had to be disengaged from the distractor and reoriented to the target location. Reorientation of voluntary attention periodically involves V1/V2 at the theta frequency. These results suggest that TMS probes theta phase-reset by attentional reorienting and help link periodic sampling in time and attention reorienting in space.

Figure 1. Experimental Paradigm

(A) Phosphene mapping session. Observers were stimulated in either the right or left occipital pole and drew their perceived phosphene. The phosphene region (“stimulated region”) and the symmetric region in the contralateral visual field (“non-stimulated region”) were used in the main experiment to determine the stimulus location. (B) Individuals’ phosphenes. Each box represents the phosphenes of one observer. Each translucent shape represents a phosphene drawing for one TMS session. (C) Trial sequence in both the psychophysics and TMS sessions. (D) Each dot represents d′ max (d′ at asymptotic performance) for a single observer in the valid condition plotted as a function of the d′ max in the invalid condition. Dots above the diagonal indicate that performance was higher for the valid than invalid cueing conditions.

Figure 2. TMS Modulates Performance

(A) Possible TMS stimulation delays on any given trial. During the TMS session, a double pulse (25 ms interval) was applied over the occipital pole at one of ten possible delays, two before and eight after the stimuli display onset. (B) Four experimental conditions: (1) valid target-stimulated, (2) valid distractor-stimulated, (3) invalid target-stimulated, and (4) invalid distractor-stimulated. (C) d′ max as a function of time, for the four experimental conditions; color schema as in (B). Error bars on plots are ±1 SEM.

Figure 3. TMS Modulation Is Periodic

(A) Difference in d′ max (normalized) performance between target-stimulated and distractor-stimulated experimental conditions, for both valid (teal) and invalid (magenta) cue condition trials. Error bars on plots are ±1 SEM. (B) Amplitude spectra obtained from an FFT performed separately on the d′ difference between stimulation conditions (solid lines) for the valid and invalid cue condition trials. The colored background corresponds to the level of significance obtained by a Monte Carlo procedure, under the null hypothesis that the d′ difference does not vary over time. The dashed line corresponds to the amplitude spectrum performed on the surrogate data obtained with the Monte Carlo procedure. The significant peak at 5 Hz in the invalid condition indicates that the magenta curve in (A) is periodically modulated at this specific frequency. (C) Amplitude spectrum obtained from an FFT performed separately on the four trial conditions (see Figure 2B): target-stimulated or distractor-stimulated, separately for valid and invalid. The same convention is used for the colored background as in (B). The significant peak at 5 Hz in the invalid condition indicates that both the invalid target-stimulated (red) and distractor-stimulated (pink) curves in Figure 3C are periodically modulated at this specific frequency. (D) Average phase difference of the 5 Hz component between target-stimulated and distractor-stimulated conditions across observers, specifically for the invalid condition. The gray area corresponds to ±1 SEM. The phase difference indicates a significant phase shift between the two curves, i.e., the invalid target-stimulated (red) and distractor-stimulated (pink) curves in Figure 3C.

Figure 4. Amplitude of Each Frequency Component for Individual Observers

An FFT was performed for each observer separately for all four conditions (see Figure 3C). Each black dot represents the amplitude of each frequency component for a given observer, averaged across target-stimulated and distractor-stimulated conditions. Only the amplitude of the 5 Hz component was significantly higher in the invalid than the valid cue condition.