Contribution of FEF to attentional periodicity during visual search: a TMS study

Visual search, looking for a target embedded among distractors, has long been used to study attention. Current theories postulate a two-stage process in which early visual areas perform feature extraction, while higher-order regions perform attentional selection. Such a model implies iterative communication between low- and high-level regions to sequentially select candidate targets in the array, focus attention on these elements, and eventually permit target recognition. This leads to two predictions: (1) high-level, attentional regions and (2) early visual regions should both be iteratively (periodically) involved during the search. Here, we used Transcranial Magnetic Stimulation (TMS) applied over the Frontal-Eye Field (FEF), known to be involved in attentional selection, at various delays while observers performed a difficult, attentional search task. We observed a periodic pattern of interference at 7 Hz (theta) suggesting that the FEF is periodically involved during this difficult search task. We further compared this result with two previous studies (Dugué et al., 2011; 2015a) in which a similar TMS procedure was applied over the early visual cortex (V1) while observers performed the same task. This analysis revealed, for both studies, the same pattern of interference, i.e. V1 is periodically involved during this difficult search task, at the theta frequency. Together, these converging findings confirm our predictions that difficult search is supported by the periodic involvement of both low- and high-level regions, at the theta frequency. Significant statement Attention models postulate a two-stage process during visual search in which early visual regions perform feature extraction, while higher-order regions perform attentional selection, these two levels iteratively (periodically) communicating until target recognition. Using TMS, we tested whether there is a causal link between both attentional and early visual regions, and attentional search performance. We showed that a difficult, attentional search is supported by the periodic involvement of both V1 and the FEF, at the theta frequency (∼6-7 Hz). This finding support the idea that visual search tasks are processed by a hierarchical system involving periodic, iterative connections between low- and high-level regions allowing successful attentional exploration.