Blood oxygenation level-dependent contrast response functions identify mechanisms of covert attention in early visual areas

Abstract

Covert attention can lead to improved performance in perceptual tasks. The neural and functional mechanisms of covert attention are still under investigation. Using both rapid event-related and mixed designs, we measured the blood oxygenation leveldependent functional MRI contrast response functions over the full range of contrast (0 -100%) in the retinotopically defined early visual areas (V1, V2, V3, V3A, and V4) in humans. Covert attention increased both the baseline activities and contrast gains in the five cortical areas. The effect on baseline can be decomposed into a transient trial-by-trial component and a component across an entire attention block. On average, increase in contrast gain accounted for Ϸ88.0%, 28.5%, 12.7%, 35.9%, and 25.2% of the trial-by-trial effects of attention in the five areas, respectively, and 22.2%, 12.8%, 7.4%, 19.7%, and 17.3% of the total effects of attention in those areas, consistent with single-unit findings in V4 and MT. The results provide strong evidence for a stimulus enhancement mechanism of attention as demonstrated in various behavioral studies.contrast gain ͉ increased baseline ͉ response gain ͉ stimulus enhancement C overt attention can lead to improved performance accuracy and response time (1, 2). Since the initial discovery that attention increases the blood oxygenation level-dependent (BOLD) responses in early visual areas (3-9), a large number of new studies have further documented many interesting effects of attention in the visual pathway, including attentional modulation of the BOLD responses in the lateral geniculate nucleus (10), increased BOLD activities in the visual cortical areas corresponding to the attended spatial location in the absence of visual stimulation (6,11,12), different effects of endogenous and exogenous attention (13,14), and topographic maps of visual spatial attention in parietal cortex (15). How attention enhances visual stimuli in early visual cortical areas, however, remains unclear. We attempt to address this fundamental question in this study.There are three potential mechanisms underlying the increased BOLD responses in early visual areas ( Fig. 1): increased contrast gain, increased response gain, and increased baseline activity. Formulated in terms of the impact of attention on contrast response functions (CRFs), these three mechanisms have distinct behavioral and functional significance. In the behavioral domain, a theoretical framework based on analyses of human observers distinguishes three mechanisms of attention: stimulus enhancement, external noise exclusion, and nonlinearity change (16,17). Whereas an increase in baseline activity need not contribute to improved discrimination and cannot be observed in psychophysical studies (18), increased contrast gain (18, 19) is related to behaviorally identified stimulus enhancement in a discrimination task, and response gain corresponds to nonlinearity changes observed behaviorally (20). Because most of the functional MRI (fMRI) attention studies used a single stimulus contrast, t...

The Attentional Field Revealed by Single-Voxel Modeling of fMRI Time Courses

“…Dumoulin and Wandell (2008) have emphasized that the BOLD HRF is "the most important non-neural influence on the pRF size estimate" when using a single-voxel timecourse modeling approach. Moreover, HRFs have been shown to vary considerably across subjects (Kim et al, 1997;Aguirre et al, 1998;Handwerker et al, 2004). Consequently, HRFs were measured for each voxel using the response to a brief, large-field, flickering checkerboard as previously reported (Puckett et al, 2014).…”

“…In more recent times, detailed knowledge of multiple hierarchically organized visual areas (Felleman and Van Essen, 1991) and the ubiquity of attentional effects throughout visual cortex (Kastner et al, 1998;Tootell et al, 1998;Brefczynski and DeYoe, 1999;BrefczynskiLewis et al, 2009) have begun to make it clear that the phenomenal effects of attention, including its perceptual topography, likely arise from the aggregate operation of multiple neurophysiological representations of the "window" of attention. For this reason, it is clear that no theory of visual attention will be complete unless it accounts for the working of attention in each visual area.…”

“…Both issues are exaggerated in higher order visual areas due to their smaller size (Puckett et al, 2010). Since different cortical visual areas are functionally specialized (Zeki et al, 1991;Maunsell, 1992;DeYoe and Van Essen, 1995;Haxby et al, 2001) and since attention influences processing in most, if not all, visual areas (Treue, 2001;DeYoe and Brefczynski, 2005;Li et al, 2008;Lauritzen et al, 2010;Bressler et al, 2013), a comprehensive neurophysiological model of attention must encompass the full hierarchy of cortical visual areas and their individual attentional effects.…”

Attention Differentially Modulates Similar Neuronal Responses Evoked by Varying Contrast and Direction Stimuli in Area MT

“…In humans, some fMRI studies have described contrastindependent attentional modulation of BOLD signals in visual cortex (Buracas and Boynton, 2007;Murray, 2008), while others have reported contrast-dependent modulations (Li et al, 2008; see also Ekstrom et al, 2009 in the monkey). Behavioral studies have also described both modulation types of psychometric functions (Carrasco, 2006).…”

Self-regulation of inter-hemispheric visual cortex balance through real-time fMRI neurofeedback training

“…To facilitate neurofeedback learning, participants were encouraged to covertly direct attention to the visual field contralateral to the ROI target , and to engage in visual mental imagery within that side. Visual imagery and shifting visual attention are known to activate the visual cortex in a regionally specific manner (Blankenburg et al, 2010;Bressler et al, 2008;Greenberg et al, 2010;Hopfinger et al, 2000;Kastner et al, 1999;Kosslyn et al, 2001;Lauritzen et al, 2009;Li et al, 2008;Ruff et al, 2006;Silver et al, 2005Silver et al, , 2007Slotnick et al, 2005;Stokes et al, 2009). We therefore hypothesized that exerting these cognitive strategies in a lateralized manner would recruit visual cortical regions overlapping with the ROI target and thus facilitate control over the differential feedback signal.…”