Transcranial magnetic stimulation to frontal but not occipital cortex disrupts endogenous attention

Significance

Human neuroimaging studies have revealed activity in frontal regions (e.g., FEF+) as a neural correlate of endogenous (voluntary) attention, and early visual areas (V1/V2) as neural correlates of both endogenous and exogenous (involuntary) attention. Using a causal manipulation—transcranial magnetic stimulation—we show that briefly disrupting activity in rFEF+ weakens endogenous attention’s benefits at attended and costs at unattended locations. In contrast, V1/V2 stimulation did not alter endogenous attention (although we have previously demonstrated that it eliminates effects of exogenous attention). Correspondingly, whereas stimulation to rFEF+ increased the rate of microsaccades directed toward the stimulated hemifield, occipital stimulation did not. Together, these results provide causal evidence for the role of rFEF+ but not V1/V2 in endogenous attention.

Abstract

Covert endogenous (voluntary) attention improves visual performance. Human neuroimaging studies suggest that the putative human homolog of macaque frontal eye fields (FEF+) is critical for this improvement, whereas early visual areas are not. Yet, correlational MRI methods do not manipulate brain function. We investigated whether rFEF+ or V1/V2 plays a causal role in endogenous attention. We used transcranial magnetic stimulation (TMS) to alter activity in the visual cortex or rFEF+ when observers performed an orientation discrimination task while attention was manipulated. On every trial, they received double-pulse TMS at a predetermined site (stimulated region) around V1/V2 or rFEF+. Two cortically magnified gratings were presented, one in the stimulated region (contralateral to the stimulated area) and another in the symmetric (ipsilateral) nonstimulated region. Grating contrast was varied to measure contrast response functions (CRFs) for all attention and stimulation combinations. In experiment 1, the CRFs were similar at the stimulated and nonstimulated regions, indicating that early visual areas do not modulate endogenous attention during stimulus presentation. In contrast, occipital TMS eliminates exogenous (involuntary) attention effects on performance [A. Fernández, M. Carrasco, Curr. Biol.  30, 4078–4084 (2020)]. In experiment 2, rFEF+ stimulation decreased the overall attentional effect; neither benefits at the attended location nor costs at the unattended location were significant. The frequency and directionality of microsaccades mimicked this pattern: Whereas occipital stimulation did not affect microsaccades, rFEF+ stimulation caused a higher microsaccade rate directed toward the stimulated hemifield. These results provide causal evidence of the role of this frontal region for endogenous attention.