I know where you are secretly attending! The topography of human visualattention revealed with fMRI

Ritobrato Datta, Edgar A. DeYoe

Medical College of Wisconsin, MEB-Neurolab, 8701 Watertown Plank Rd., Milwaukee, WI 53226, United States

a r t i c l e i n f o

Article history:

Received 9 May 2008Received in revised form 10 December 2008

Keywords:

Spatial attentionfMRI humanVisual cortexNeurophysiology

a b s t r a c t

Previous studies have described the topography of attention-related activation in retinotopic visual cor-tex for an attended target at one or a few locations within the subject’s ﬁeld of view. However a completedescription for all locations in the visual ﬁeld is lacking. In this human fMRI study, we describe the com-plete topography of attention-related cortical activation throughout the central 28

of the visual ﬁeld andcompare it with previous models. We cataloged separate fMRI-based maps of attentional topography inmedial occipital visual cortex when subjects covertly attended to each target location in an array of threeconcentric rings of six targets each. We combined the attentional maps for each of the 18 target locationsfor each subject into a unique composite display to identify common principles of attentional organiza-tion for different target locations. Attentional activation was universally highest at the attended targetbut spread to other segments in a manner depending on eccentricity and/or target size. For targets scaledin size with eccentricity, the attentional effects spread circumferentially as a gradient whose full width athalf maximum was consistently 1.5 times the target width at each eccentricity. For targets in the inner(1.8–8.5

) and middle (8.5–15.6

) rings, attention also tended to spread outward, radially to other seg-ments. For targets in the outer ring (15.6–28

), the radial spread of attention was primarily inward totargets of the middle ring. We propose an ‘‘attentional landscape” model that is more complex than a‘‘spotlight” or simple ‘‘gradient” model but includes aspects of both. Finally, we asked subjects to secretlyattend to one of the 18 targets without informing the investigator. We then show that it is possible todetermine the target of attentional scrutiny from the pattern of brain activation alone with 100% accu-racy. Together, these results provide a comprehensive, quantitative and behaviorally relevant account of the macroscopic cortical topography of visuospatial attention. We also show the pattern of attentionalenhancement as it would appear distributed within the observer’s ﬁeld of view thereby permitting directobservation of a neurophysiological correlate of a purely mental phenomenon, the ‘‘window of attention”.

1. Introduction

Visual attention performs a spatially selective enhancement of task-relevant information and suppression of irrelevant informa-tion thereby acting as a gateway to our awareness for potentiallysignificant locations, objects and events in the world around us( James, 1890). This ubiquitous selection process, of which the ob-server is often unaware, has been compared to a ‘‘spotlight” whichselectively illuminates objects of interest for detailed scrutiny(Posner, Snyder, & Davidson, 1980). Though the spotlight modelis attractive in its simplicity, it fails to capture the complex topog-raphy of attentional selection throughout the field of view. Psycho-physical data show that attentional enhancement is distributed asa gradient around the attended target with decreasing effects asdistance increases (Downing & Pinker, 1985). However, the datasupporting the simple gradient model typically are based on asmall number of tested locations and are averaged across multiplesubjectsthereby obscuring the truecomplexityof attentionin indi-vidual observers and for different locations throughout the field of view.Previous studies have begun to outline the neurophysiologicalbasis of this attentional selection(Bisley & Goldberg, 2006; Buracas&Boynton,2007; Bushnell, Goldberg, &Robinson,1981; Corbetta&Shulman, 1998; Desimone & Duncan, 1995; Goldberg & Bushnell,1981; Kastner & Pinsk, 2004; Kastner, Pinsk, De Weerd, Desimone,& Ungerleider, 1999; Liu, Larsson, & Carrasco, 2007; Martinez et al.,2001; Maunsell & Treue, 2006; Moran & Desimone, 1985; Motter,1993; Reynolds & Chelazzi, 2004; Saenz, Buracas, & Boynton,2002; Silver, Ress, & Heeger, 2006; Treue & Martinez Trujillo,1999; Williford & Maunsell, 2006). FMRI experiments with humansubjects have shown that attention directed to a specific location

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deyoe@mcw.edu(E.A. DeYoe).Vision Research 49 (2009) 1037–1044

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Vision Research

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or object results in enhancement of visual cortex activity at retino-topically mapped sites representing the location of the covertly at-tended target within the visual ﬁeld (Brefczynski & DeYoe, 1999;Gandhi, Heeger, & Boynton, 1999; Somers, Dale, Seiffert, & Tootell,1999). However, a deﬁnitive test of the accuracy of this neuro-physiological mechanism has not been performed previously. Herewe report the results of such a test in which we used fMRI to cat-alog the attentional patterns in medial occipital cortex (V1/V2) forall potential target locations within a dartboard-like array of 18segments extending 28

into the peripheral visual field. fMRIexperiments with individual subjects confirm that attentional ef-fects spread to areas surrounding an attended target but show thatmore remote locations can exhibit weak attentional effects as well(Brefczynski, Datta, Lewis, & DeYoe, 2009; Tootell et al., 1998).While it is clear that the overall topography of attention varieswith attended target location, a comprehensive account of thesechanges for all visual field locations has been lacking. We per-formed a combined analysis of the cataloged data from the previ-ously mentioned experiment and used it to identify universalfeatures of attentional topography for all visual field locations. Fi-nally, in order to crosscheck the behavioral validity of the atten-tional topography, we performed a blind study in which thesubjects covertly attended to a target which they selected in secret.We then used the fMRI brain activation to make predictions aboutthe secretly attended target thereby providing a test of the behav-ioral relevance of the fMRI data.

2. Methods

2.1. Subjects

Four subjects (two male, two female) drawn from the popula-tion of Medical College of Wisconsin participated in this study. In-formed consent was obtained from all the subjects in accordancewith procedures and protocols approved by the Medical Collegeof Wisconsin internal review committee.

2.2. fMRI data acquisition

Scanning was performed on a 1.5 Tesla or 3 Tesla General Elec-tric ‘‘Signa” scanner at the Medical College of Wisconsin. A custom-ized RF/Gradient head coil and a gradient echo pulse sequence(TE = 40 ms, TR = 2 s, FA = 90

for 1.5 T and TE = 30 ms, TR = 2 s,FA = 77

for 3T) were used. Time series of 128 echo planar imageswere acquired with 3.75

3.75

4.0 mm resolution. Thirty oneslices spanning the occipito-temporal cortex were collected inthe axial plane. Anatomical images were obtained using a T1-weighted spoiled GRASS (gradient recalled at steady state) pulsesequence at a resolution of 256

192

1.1 mm. For the functionalMRI scans, subjects used a custom-designed optical system to viewa computer graphics stimulus array generated with a Cambridgeinstruments VSG video board driving a modiﬁed Sharp XG-2000Uvideo projector. The optical system allowed a large ﬁeld of viewsubtending 56

of visual angle (28

radius).

2.3. Attentional mapping 2.3.1. Visual stimulus

ThestimulusarraydepictedinFig.1,consistedofacounterphaseflickering(6 Hz)dartboard-likearraycontainingasmallcentralseg-ment surrounded by 18 segments arranged in three concentric cir-cles. A white fixation marker was superimposed on the center of thedisplay.Thesizesandstripeperiodsofthesegmentswerevariedwitheccentricitytoroughlycompensateforcorrespondingchangesincorticalmagnificationfactorandspatialacuity.Thestimuluswasdisplayed on a back-projection screen and viewed by the subjectwithin the MRI scanner via custom-designed binocular optics witha 56

ﬁeld of view. The radius of the central segment in the viewedimage subtended 1.8

of visual angle. The segments of the inner,middle, and outer rings extended radially from 1.8

to 8.5

; 8.5

to15.6

and 15.6

to 28

, respectively. The blue and orange stripe col-orswereselectedtobeapproximatelycomplementaryandweread- justedto appear matched in relative brightness. Color differenceswere clearly evident even at the largest eccentricities. Mean lumi-nance of the entire stimulus array was approximately 20 cd/m

and matched the luminance of the uniform gray screen ﬁlling theremainderofthedisplay.Ambientlightwithintheboreofthescan-ner was effectively zero and the stimulus array ﬁlled the circularapertureoftheoptics.Every2 s,thecolorsand/orstripeorientationsof all segments changed randomly. Statistically, all segments wereindistinguishable with respect to the mean number of occurrencesof each color/orientation combination.

2.3.2. Task (Fig. 1)

During fMRI, subjects were instructed to maintain fixation onthe central marker throughout the entire scan. We verified fixationcompliance outside the scanner using the identical stimulus/taskand an optical eyetracker. During the scan, prearranged audio cues(‘‘zero”or ‘‘one”)presentedevery 2 s via customelectrostatichead-phones (Koss Inc.) instructed the subjects to covertly attend toeither the center stimulus segment (cue 0) or a prearrangedperipheral segment (cue 1). Cueing conditions were grouped into6 s. blocks of either the 0 or 1 condition presented on three succes-sive 2-s trials. Cue conditions were then randomized across blocksthroughout each 276 s fMRI scan, which began with a 20s period of passive fixation. Typically, five fMRI scans were repeated and aver-aged to increase contrast-to-noise. During both cue conditions, thesubject was required to press one of two buttons on every trial toindicate the color/orientation conjunction at the cued segment(Button A: blue-horizontal or orange-vertical versus Button B:blue-vertical or orange-horizontal). This feature conjunction taskensured that focal attention was engaged and directed towardthe cued segment since the conjunction cannot be reported cor-rectly if attention is directed elsewhere (Treisman, 1982). Impor-tantly, no visual aspect of the stimulus array could be used touniquely identify the attended segment. In a single scan session,the subject was cued to attend to only one of the 18 segments. Atotal of 18 scan sessions were performed with each subject to

Fig. 1.

Stimulus and task description. The stimulus consists of a central segmentsurrounded by 18 peripheral segments arranged in three concentric rings. Subjectsﬁxate center marker continually. Auditory cues direct the subject to attend to thecenter segment or, alternately, to a prearranged peripheral segment in a random-ized block design. On each 2 s trial, subjects must detect color + orientationconjunction at the cued segment. (see online publication for color ﬁguresthroughout the paper.)1038

R. Datta, E.A. DeYoe/Vision Research 49 (2009) 1037–1044

catalog the attention-related activation for each of the 18 seg-ments, thereby yielding a complete library of attentional patterns.In addition, separate scan sessions were performed in which thesubjects randomly chose a target and covertly attended to it with-out informing the experimenter of the choice. After the scan ses-sion, subjects did not reveal the identity of the secretly attendedsegment until after all analysis of the fMRI data had been per-formed, thereby ensuring an unbiased prediction of the attendedtarget.

2.4. Retinotopic mapping 2.4.1. Stimuli

As outlined inFig. 2a and b, conventional eccentricity mapping(DeYoe et al., 1996) was accomplished with a counterphase ﬂicker-ing(8 Hz),checkeredannulusthatslowlyexpandedfromthecenterof gaze to 28

over a period of 40 s. The expansion steps, inner andouter diameter and check size were all scaled in proportion to themean eccentricity of the annulus. To map visual field polar angle,a checkered hemifield slowly rotated about the center of gaze. Bothannulusexpansionandhemifieldrotationsequenceswererepeatedthree times during each fMRI scan. Each stimulus evoked waves of activation that moved through the visual cortex, activating succes-sive retinotopic positions at different times (temporal phases) rela-tive to the beginning of the stimulus cycle. In this manner, theretinal position of the stimulus that optimally activated a corticallocuscouldbedeterminedfromthetimedelayofitsfMRIresponse.Valid responses were identified using a modification of a standardtemporal cross-correlation method (Bandettini, Jesmanowicz,Wong, & Hyde, 1993; Saad, DeYoe, & Ropella, 2003). The modifiedalgorithm efficiently identified the optimal temporal phase, cross-correlation coefficient, and the magnitude of the response.

2.5. fMRI post processing

Raw fMRI data were converted to images using a custom recon-struction technique (Bandettini et al., 1993). The resulting imageswere assembled into volumetric datasets and further processedusing the AFNI analysis package (Cox, 1996). Typically, individualimages within the volumetric dataset were co-registered to reducemotion artifacts. As the experiments were semi-randomizedblocked designs, the analysis consisted of a multiple regressionanalysis of the fMRI time series data with regressors including amean and linear trend (nuisance variables) and the time se-quences of the experimental conditions after convolution with agamma function model of the hemodynamic response function.We used the linear scaling coefﬁcients (AFNI LC

parameters) of the regression analysis with their corresponding

-statistics and

-values as a measure of fMRI amplitude for each experimentalcondition.

2.6. Region of analysis

Subsequent analyses were restrictedto the set of voxels in med-ial occipital cortex corresponding to retinotopically defined visualareas V1/V2. This was accomplished by using the polar angle map-ping data to identify the borders of V1 and V2 and then creating adigital, volumetric mask to encompass both regions. We pooledvoxels from both visual areas in order to obtain a sufficiently largenumber of voxels distributed throughout the activated visual fieldfor the subsequent attentional field map analysis (see below). Inprevioustests, we have not beenable to identifyany consistent dif-ferences between the attentional topography in V1 versus V2 forthe attentional task used here (Brefczynski et al., 2009). All voxelsinside the masked region were included for further analysisregardless of their attentional amplitude measure.

2.7. Attentional ﬁeld maps

The construction of attentional ﬁeld maps (AFMaps) is outlinedinFig. 2. The AFMap is a computational back-projection of the cor-tical pattern of attention-related fMRI activation onto a diagram of the subject’s ﬁeld of view thereby permitting visualization of the

Fig. 2.

Construction of AFMaps and contour maps. (a) Expanding ring retinotopy experiment identifies the stimulus eccentricity (rho) that maximally activated eachretinotopically selective voxel. (b) Rotating Hemifield retinotopy experiment identifies the polar angle (theta) of the stimulus that maximally activated each voxel. (c)Attentional experiment measures the attentional modulation for each voxel. (d) AFMap ‘‘back-projection” of all visually responsive voxels in medial occipital cortex onto thesubject’s visual field that is covered by thetarget array. For each visually responsive brain voxel, a circle symbol is placed on a diagram of the visual field based on its preferredeccentricity and polar angle. The size of the symbol represents the experimental error in locating the preferred position. The symbol is colored to represent the normalizedamplitude of the attentional modulation for that voxel. Yellow/red colors indication activation while blue colors represent suppression. No statistical thresholding wasapplied. (See text for more details.) (e) Contour map in which

’s indicate locations of data-points representing the average attentional modulation of all voxels whose centersfall within the corresponding stimulus segment (indicated by gray overlaid grid). Data for the 18 individual points were then ﬁt with a smoothed and interpolated surfaceviewed here as a contour map.

R. Datta, E.A. DeYoe/Vision Research 49 (2009) 1037–1044

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I know where you are secretly attending! The topography of human visual attention revealed with fMRI

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Vision Res. 2009 May;49(10):1037-44.

Datta R, DeYoe EA.

Previous studies have described the topography of attention-related activation in ret... (More)