Transcranial Magnetic Stimulation Reveals Attentional Feedback to Area V1 during Serial Visual Search

Laura Dugué,Rufin Vanrullen,Philippe Marque,Michael H Herzog

doi:10.1371/journal.pone.0019712

Abstract

Visual search tasks have been used to understand how, where and when attention influences visual processing. Current theories suggest the involvement of a high-level “saliency map” that selects a candidate location to focus attentional resources. For a parallel (or “pop-out”) task, the first chosen location is systematically the target, but for a serial (or “difficult”) task, the system may cycle on a few distractors before finally focusing on the target. This implies that attentional effects upon early visual areas, involving feedback from higher areas, should be visible at longer latencies during serial search. A previous study from Juan & Walsh (2003) had used Transcranial Magnetic Stimulation (TMS) to support this conclusion; however, only a few post-stimulus delays were compared, and no control TMS location was used. Here we applied TMS double-pulses (sub-threshold) to induce a transient inhibition of area V1 at every post-stimulus delay between 100 ms and 500 ms (50 ms steps). The search array was presented either at the location affected by the TMS pulses (previously identified by applying several pulses at supra-threshold intensity to induce phosphene perception), or in the opposite hemifield, which served as a retinotopically-defined control location. Two search tasks were used: a parallel (+ among Ls) and a serial one (T among Ls). TMS specifically impaired the serial, but not the parallel search. We highlight an involvement of V1 in serial search 300 ms after the onset; conversely, V1 did not contribute to parallel search at delays beyond 100 ms. This study supports the idea that serial search differs from parallel search by the presence of additional cycles of a select-and-focus iterative loop between V1 and higher-level areas.

Highlights

For more than thirty years, and in particular since the precursory studies by Treisman and Gelade (1980) [1], visual search experiments have been used to study attention [1,2,3,4]
In a preliminary experiment on the same group of subjects (n = 12) that participated in the main experiment, we determined search slopes for the two tasks that we intended to use in the main experiment: finding the letter T among Ls, and finding the symbol + among Ls
One notable aspect of our results is that the administration of Transcranial Magnetic Stimulation (TMS) over occipital cortex induced non-specific biases that could have been mistaken for attentional effects

Summary

Introduction

For more than thirty years, and in particular since the precursory studies by Treisman and Gelade (1980) [1], visual search experiments have been used to study attention [1,2,3,4]. If the selected location does not correspond to the target, the system iterates by selecting the most salient location and re-focusing attentional resources, until the target is found In this model the difference between parallel and serial tasks has a physiological correlate in the feedback projections from high-level areas, redistributing the contents of the master location map to lowlevel areas and feature maps. This interaction between higher-level and lower-level areas should be persistently active during serial search until the target is found, whereas for parallel search it should vanish quickly after stimulus onset (since finding the target would only require a single feed-forward pass through the system). The present study was designed to test this hypothesis using Transcranial Magnetic Stimulation (TMS)

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Conclusion