Why does neuronal activity in sensory brain areas sometimes give rise to perception, and sometimes not? Although neuronal noise is often invoked as the key factor, a portion of this variability could also be due to the history and current state of the brain affecting cortical excitability. Here we directly test this idea by examining whether the phase of prestimulus oscillatory activity is causally linked with modulations of cortical excitability and with visual perception. Transcranial magnetic stimulation (TMS) was applied over human visual cortex to induce illusory perceptions (phosphenes) while electroencephalograms (EEGs) were simultaneously recorded. Subjects reported the presence or absence of an induced phosphene following a single pulse of TMS at perceptual threshold. The phase of ongoing alpha (ϳ10 Hz) oscillations within 400 ms before the pulse significantly covaried with the perceptual outcome. This effect was observed in occipital regions around the site of TMS, as well as in a distant frontocentral region. In both regions, we found a systematic relationship between prepulse EEG phase and perceptual performance: phosphene probability changed by ϳ15% between opposite phases. In summary, we provide direct evidence for a chain of causal relations between the phase of ongoing oscillations, neuronal excitability, and visual perception: ongoing oscillations create periodic "windows of excitability," with sensory perception being more likely to occur at specific phases.
Visual search--finding a target element among similar-looking distractors--is one of the prevailing experimental methods to study attention. Current theories of visual search postulate an early stage of feature extraction interacting with an attentional process that selects candidate targets for further analysis; in difficult search situations, this selection is iterated until the target is found. Although such theories predict an intrinsic periodicity in the neuronal substrates of attentional search, this prediction has not been extensively tested in human electrophysiology. Here, using EEG and TMS, we study attentional periodicities in visual search. EEG measurements indicated that successful and unsuccessful search trials were associated with different amounts of poststimulus oscillatory amplitude and phase-locking at ∼6 Hz and opposite prestimulus oscillatory phase at ∼6 Hz. A trial-by-trial comparison of pre- and poststimulus ∼6 Hz EEG phases revealed that the functional interplay between prestimulus brain states, poststimulus oscillations, and successful search performance was mediated by a partial phase reset of ongoing oscillations. Independently, TMS applied over occipital cortex at various intervals after search onset demonstrated a periodic pattern of interference at ∼6 Hz. The converging evidence from independent TMS and EEG measurements demonstrates that attentional search is modulated periodically by brain oscillations. This periodicity is naturally compatible with a sequential exploration by attention, although a parallel but rhythmically modulated attention spotlight cannot be entirely ruled out.
SUMMARY 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.
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