Preparatory deployment of attention to motion activates higher-order motion-processing brain regions

www.elsevier.com/locate/ynimg NeuroImage 22 (2004) 1515 – 1522

Preparatory deployment of attention to motion activates higher-order motion-processing brain regions Tracy L. Luks * and Gregory V. Simpson Dynamic NeuroImaging Laboratory, Department of Radiology, University of California San Francisco, San Francisco, CA 94143-0926, USA Received 30 October 2003; revised 13 April 2004; accepted 15 April 2004

We used event-related fMRI to test the hypothesis that preparatory attention modulations occur in higher-order motion-processing regions when subjects deploy attention to internally driven representations in a complex motion-processing task. Using a cued attention-to-motion task, we found preparatory increases in fMRI activity in visual motion regions in the absence of visual motion stimulation. The cue, a brief enlargement of the fixation cross, directed subjects to prepare for a complex motion discrimination task. This preparation activated higher-order and lower-order motion regions. The motion regions activated included temporal regions consistent with V5/MT+, occipital regions consistent with V3+, parietal-occipital junction regions, ventral and dorsal intraparietal sulcus, superior temporal sulcus (STS), posterior insular cortex (PIC), and a region of BA 39/40 superior to V5/MT+ involving the angular gyrus and supramarginal gyrus (ASM). Consistent with our hypothesis that these motion sensory activations are under top-down control, we also found activation of an extensive frontal network during the cue period, including anterior cingulate and multiple prefrontal regions. These results support the hypothesis that anticipatory deployment of attention to internally driven representations is achieved via top-down modulation of activity in task-relevant processing areas. D 2004 Elsevier Inc. All rights reserved. Keywords: fMRI; Attention; Motion

Introduction In the real world, we sometimes deploy our attention to an object present in the visual scene in anticipation that it may move or change. This involves the interaction of top-down attentional deployment mechanisms with externally driven representations of sensory input. In other instances, we deploy our attention to things that are not present, but will occur later. This involves the interaction of top-down processes with internally generated representations of to-be-attended objects. In the present study, we have eliminated visual information from the scene to ensure complete reliance on internally generated representations. We investigated * Corresponding author. Dynamic NeuroImaging Laboratory, Department of Radiology, University of California San Francisco, Box 0946, San Francisco, CA 94143-0926. Fax: +1-415-514-0405. E-mail address: [email protected] (T.L. Luks). Available online on ScienceDirect (www.sciencedirect.com.) 1053-8119/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2004.04.008

whether top-down attentional deployment can activate high-order visual motion areas when attention is cued to complex visual motion in the absence of stimuli. Attention to an externally driven representation is often thought of as a modulation of sensory processing that preferentially enhances task-relevant representations and inhibits other information. This modulation may be accomplished by an attention network, involving prefrontal, parietal, and cingulate cortical areas (e.g., Mesulam, 1981; Posner and Peterson, 1990). Enhanced visual sensory cortical activity to attended visual stimuli, relative to unattended visual stimuli, has been observed at all levels of brain imaging, from the action potentials of single neurons to EEG to PET and fMRI. Enhanced sensory responses have been recorded in the earliest visual cortical regions and in regions that are responsible for processing specific features of visual stimuli under a broad spectrum of visual conditions (Pessoa et al., 2003, review). Modulation of sensory responsiveness may serve to bias activity in favor of attended items in the visual scene (e.g., Desimone and Duncan, 1995). A question of importance for attentional deployment is whether similar mechanisms are used when the target of attention is an internally generated representation (i.e., no stimulus is present). The few studies that have addressed this issue have provided evidence for deployment via activation of internally generated representations of the to-be-attended stimulus features (similar to that found for externally driven representations). This has been found for deployment to space, object, and color, but not for deployment to motion (Driver and Frackowiak, 2001, review). In a visual pattern discrimination task, Kastner et al. (1998, 1999) reported selectively enhanced activity in V1, V2, V4, and TEO corresponding to the location of the to-be-attended stimulus during a preparatory period in the absence of visual stimuli. Similarly, sensory activations have been reported in response to spatial and non-spatial feature attention cues, before target stimulus presentation (e.g., Corbetta et al., 2000; Giesbrecht et al., 2003; Hopfinger et al., 2000; Macaluso et al., 2003; O’Connor et al., 2003). These results provide evidence for preparatory top-down ‘‘biasing’’ of internally generated representations of color, object, and space. We examined whether similar top-down preparatory modulations occur in higher-order motion-processing regions when subjects deploy attention to internally generated representations in a complex motion-processing task. Two studies have examined preparatory deployment of attention to motion under externally driven conditions in which relevant

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sensory inputs are present. Chawla et al. (1999) reported increased V5/MT+ activation while subjects attended a static dot array and prepared for a motion discrimination, relative to preparation for a color discrimination. Shulman et al. (1999) reported activity in areas V5/MT+, intraparietal sulcus (IPS), and lateral occipital cortex while subjects attended a directional arrow cue and a randomly moving dot array, in preparation for brief coherent movement of a subset of dots in the target direction. In the present study, we used fMRI to investigate the network of frontal, parietal, and sensory regions underlying transient deployment of attention to complex motion in the absence of relevant sensory inputs. We test the hypothesis that preparatory attention modulations occur in higher-order motion-processing regions purely via top-down control.

Materials and methods Subjects Twelve subjects (eight men and four women) participated in this research. These subjects were 25 – 40 years old, right-handed, with graduate or post-graduate education levels. All had normal or corrected-to-normal vision and had no reported history of head trauma or neurological disorders. All subjects gave written in-

formed consent and were screened for MRI eligibility in accordance with guidelines established by the UCSF Committee on Human Research. Task methods The task consisted of a cued-motion discrimination task (Fig. 1). Subjects were given training on how to monitor a rapid series of 10 stimuli with different types of radial motion for a particular target motion. Before each fMRI acquisition, subjects were presented with their type of target motion and were instructed to attend to the left or right visual field (LVF or RVF) for that entire block of six trials. Order of visual field attention was randomized. Each trial began with a 10-s fixation stimulus, a white ‘‘+’’ on a black background, subtending 1j of visual angle. This fixation period was followed by the cue (a slight enlargement of the fixation ‘‘+’’ for 250 ms (1.5j), after which the ‘‘+’’ returned to its original size). This cue indicated that the series of different motion stimuli would appear soon, and subjects should prepare to discriminate between the upcoming motion stimuli to detect their target type of motion in the attended visual field and to ignore any stimuli presented in the unattended visual field. After an ISI of either 9.75 or 1.25 s (see below), a series of 10 motion stimuli were presented (each 350-ms duration, 650-ms ISI, creating a 10-s block of stimulation). Each stimulus consisted of a single circular patch of white dots with

Fig. 1. Experimental design of the behavioral task. Block instructions directed attention to the left or right. Enlargement of the fixation cross on each trial cued subjects to prepare for motion stimuli. A series of 10 motion stimuli was monitored for a type of target motion if they appeared in the attended visual field.

T.L. Luks, G.V. Simpson / NeuroImage 22 (2004) 1515–1522

coherent motion varying in spiral 3D direction (left, right, or no rotation; contraction, expansion, or none). The diameter of the circular patch was 6j, dot size was 0.15j, and the density of dots was 0.8 dots per degree. Movement within each stimulus was created by displaying six images for 50 ms, with 10 ms between images, in which rotation or dilation occurred at 0.25j per image. One to three of the 10 stimuli were the target pattern (i.e., right rotating and expanding). All 10 stimuli within each trial were presented in the same location, centered at 6j in the lower left or right visual quadrant. On each trial, this series of motion stimuli was presented in either the attended or unattended visual field (50% probability). For example, for a given block, subjects were instructed to attend to the LVF, and three trials would be presented on the left and three on the right, randomly. If the stimuli appeared in the attended visual field, the subject monitored the series for the particular target motion pattern and responded. Responses were made by a right index finger press on the response pad. If the stimuli appeared in the unattended visual field, the subject ignored them. The ISI was randomly set at 9.75 s on 4/5 of the trials and 1.25 s on 1/5 of the trials. These shorter ISI trials were used as ‘‘catch trials’’ to encourage subjects to prepare for the motion stimuli immediately following the cue on all trials, even though on most trials, the stimuli were not presented for almost 10 s. This was intended to increase the detectability of preparation during the cue period by encouraging immediate preparation, but allowing sufficient time on most trials between the cue and motion stimuli to distinguish the blood-oxygen-level-dependent (BOLD) response to preparation from the BOLD response to the motion stimuli. Stimulus presentation and experiment control Visual stimuli were presented with PsyScope 1.2.5 on an Apple Macintosh PowerPC running MacOS9 and projected using an LCD video projector onto a back-projection screen located at the foot of the scanner table. Subjects viewed the screen using a mirror attached to the head coil. Subjects made finger-press responses on a fiber-optic eight channel response pad (Lightwave Medical Industries Ltd., Vancouver, BC). The response pad device also collected scanner TTL pulses generated at the onset of each image acquisition. Scanner signals were then input to a PsyScope button box and recorded by the PsyScope presentation program. The PsyScope software generated a data file containing recorded event times for all stimulus presentation events, subject responses, and scanner TTL pulse events. This allowed for precise retrospective temporal synchronization of stimulus events and image acquisition.

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Data analysis Image analysis was performed on a Sun Ultra 10 workstation (Sun Microsystems) using MATLAB (Mathworks Inc.) and SPM99 software (www.fil.ion.ucl.ac.uk/spm). Before analysis, the functional images were converted to 3D Analyze format volumes. The first four volumes in each run were discarded. Images were realigned to the 5th volume within each run to correct for motion artifacts using a six-parameter rigid body affine transformation. The resulting images were normalized to a standard stereotaxic space (Montreal Neurological Institute (MNI) Template) using a 12-parameter affine/non-linear transformation and spatially smoothed with an 8-mm full-width half maximum isotropic Gaussian kernel. Image intensity was scaled to the mean global intensity of each time series. Data were submitted to a mixed-design General Linear Model analysis, fitting a reference hemodynamic response function (hrf) to the observed time series data. Fixation and motion stimuli conditions were modeled as epochs convolved with the hrf (fixation = 10 s epoch, motion stimulus period = 11 s epoch), and cues were modeled as events (essentially, 0 s epochs). For trials with 1.25 s ISIs, the cue and motion stimuli were modeled as a single epoch of 12 s, convolved with the reference hrf, because we were not interested in distinguishing the cue and motion stimuli contributions of these trials to the BOLD signal, but wanted to treat these trials as effects of noninterest. Thus, there were the following conditions: left cue, right cue, attended left motion, attended right motion, unattended left motion, unattended right motion, fixation, short ISI attended right motion, short ISI attended left motion, short ISI unattended right motion, and short ISI unattended left motion. Contrasts of interest were performed on individual subject data. Each experimental condition of interest was individually compared with the fixation condition. To examine the effects of attention on motion stimulus processing, we also compared responses to the attended and unattended motion stimuli for each visual field. For each contrast at the individual level, statistical parametric brain maps were generated that displayed the t value (in signal intensity) of each voxel that met a threshold of P < 0.001 uncorrected for multiple comparisons. Second-level one-sample t tests were performed on the combined individual results to create random-effect group analyses for each contrast (n = 12). For each contrast at the group level, statistical parametric brain maps were generated that displayed the t value (in signal intensity) of each voxel that met a threshold of P < 0.001 uncorrected for multiple comparisons. For both group and individual level results reported here, these images were overlaid onto SPM99’s single-subject canonical T1 image in MNI space. Stereotaxic coordinates reported here were converted to approximate Talairach space from MNI coordinate space (www.mrc-cbu.cam.ac.uk/Imaging/mnispace.html).

Magnetic resonance methods Motion-processing regions Imaging was performed on a 1.5-T General Electric Signa LX 8.3 scanner (Milwaukee, WI). Anatomical imaging consisted of a high-resolution T1-weighted rf-spoiled GRASS sequence (SPGR). Functional imaging consisted of blood-oxygen-level-dependent (BOLD) sensitive images (Kwong et al., 1992; Ogawa et al., 1990) acquired during performance of the experimental task using a gradient-recalled echo-planar (EPI) sequence (TR = 3 s; TE = 50 ms; flip angle = 60, matrix = 128  128, FOV = 26  26 cm, 19 slices, 5-mm thickness, 1 mm gap).

We identified the locations of fMRI activity according to the location of each peak activation for each cluster of significant voxels (or each local maxima within a cluster greater than 8 voxels apart). We assigned fMRI activations to the following motionrelated areas according to Talairach coordinates derived from the visual motion literature (Tootell et al., 1995a,b; Watson et al., 1993; Zeki et al., 1991; for review, see Sunaert et al., 1999): V3+, parietal-occipital sulcus (SPO), parietal-occipital sulcus where it

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Table 1 Labeling of activations as motion-related areas

Table 2 Cue period group activations

Region

Comparison Location of interest

Talairach coordinates X

V5/MT+ V3+ SPO VIPS POIPS STS PIC A-SM DIPSL DISPA

Left Right Left Right Left Right Left Right Left Right Left Right Left Right Left Right Left Right Left Right

Y

Z

46 ( 40; 54) 42 (40;44) 22 ( 6: 26) 15 (9;24) 11 ( 7; 15) 15a 29 ( 28; 34) 27 (25;31) 22a 12 (10;17) 58 ( 55; 63)

61 ( 57; 66) 65 ( 65; 68) 77 ( 67; 81) 73 ( 67; 83) 71 ( 67; 80) 72a 71 ( 61; 79) 66 ( 60; 70) 64a 58 ( 56; 64) 51 (42; 60)

4 ( 8;8) 3 ( 3;3) 11 (9;13) 15 (11;17) 28 (24;34) 30a 35 (27;42) 38 (35;44) 42a 40 (38;41) 19 (14;19)

54 ( 44; 60) 40 (32;47) 46 ( 41; 49) 44 (32;47) 30a 27a 35 ( 22; 42) 19a

31 ( 41 ( 57 ( 55 ( 54a 63a 38 ( 38a

31 (30;34) 28 (28;29) 35 (28;40) 34 (28;43) 62a 59a 55 (52; 61) 56a

23; 39; 51; 52;

40) 43) 64) 61)

38; 42)

Median and 1st, 3rd quartile Talairach coordinates of activation peak voxels within each anatomical motion-processing category, across all comparisons of interest. Left/Right = left and right hemispheres; SPO = parietal occipital sulcus; VIPS = ventral intraparietal sulcus; POIPS = parietal occipital intraparietal sulcus junction; STS = superior temporal sulcus; PIC = posterior insular cortex; A-SM = angular/supramarginal gyrus; DIPSL = dorsal intraparietal sulcus, lateral; DIPSA = dorsal intraparietal sulcus, anterior. a Denotes insufficient number of observations in this region to calculate quartiles.

Brodmann’s Talairach area coordinates X

Right cue > fixation

Left cue > fixation

A-SM Middle frontal gyrus ACC VIPS

Y

t value Z

39/40 46

57 40

49 32

23 21

32

2 30 26 46 50 32 34 4 26 14 40 30 34 22 34

43 58 71 6 1 15 8 3 4 9 38 44 8 7 46

5 4.20 42 5.12 50 4.98 43 12.99 17 6.54 52 4.04 43 7.55 57 4.14 44 4.05 60 4.33 31 4.69 27 6.10 31 6.66 17 4.70 16 7.28

Precentral gyrus 4

Middle frontal gyrus

6

Superior frontal gyrus Inferior frontal gyrus Middle frontal gyrus

9 9/47 46

6.47 4.30

All activations are significant at P < 0.001, uncorrected from multiple comparisons. Given coordinates are local maxima >8.0 mm apart within the specified region. Abbreviations as for Table 1.

and quartile Talairach coordinates of the activations assigned to each location category (across all comparisons of interest), and Fig. 2 displays those median locations.

Results meets with intraparietal sulcus (POIPS), V5/MT+, superior temporal sulcus (STS), posterior insular cortex (PIC), angular gyrus and supramarginal gyrus (A-SM), ventral intraparietal sulcus (VIPS), dorsal intraparietal sulcus, lateral (DIPSL), and dorsal intraparietal sulcus, anterior (DIPSA). Table 1 gives the median

Cue period activity We found consistent activations in frontal regions, with robust, variably located sensory activations for the cue period, when

Fig. 2. Labeling of activations as motion-related areas. Display of median Talairach coordinates of activation peak voxels within each motion-processing region, across all comparisons of interest, given in Table 1. Abbreviations as for Table 1.

T.L. Luks, G.V. Simpson / NeuroImage 22 (2004) 1515–1522 Table 3 Cue period activations for individual subjects combined across left and right cue conditions Subject no. 1 2 3 4 5 6 7 8 9 10 11 12 TOTAL

V5/MT+

V3+

L

L *

* * * * * * * *

8

R

* *

STS

R

L

R

L

*

*

*

*

*

* *

* *

*

*

*

*

*

*

*

*

*

* *

4

VIPS

* 4

5

* 4

*

4

*

4

A-SM R

SPO

POIPS L

L

R

L

R

*

*

*

*

*

*

* * *

*

*

*

*

* *

3

* * * 7

R *

*

*

* * * * 5

5

1

1

3

Talairach coordinates of each location are given in Table 1 and the locations are displayed in Fig. 2. All activations are significant at P < 0.001, uncorrected from multiple comparisons. Abbreviations as for Table 1. L = left hemisphere; R = right hemisphere; Total = total number of subjects with activation in each region.

compared to fixation. The random effects group level analysis revealed significant activations bilaterally in frontal areas BA 4, 6, 9, 32, 40, 46, and 47 (see Table 2). In sensory cortex, two significant activation clusters were observed in left VIPS for the left cue period, and one significant activation in left A-SM for the right cue period.

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During both left and right cue periods, individual subject analyses revealed significant activation in a large number of brain regions associated with higher-order visual motion processing. These included V3+, SPO, POIPS, V5/MT+, STS, PIC, A-SM, VIPS, DIPSL, and DIPSA (Table 3, Fig. 3). The exact location of activations varied across subjects. Left V5/MT+ was the most commonly activated region across subjects (8 of 11 subjects). There was no clear contralateral location effect associated with left and right cue conditions; across subjects, both cues produced bilateral activations in all these regions, with a tendency for more extensive left hemisphere activations following both right and left cues. These results suggest that preparatory attention modulations occur in higher-order motion-processing regions when subjects deploy attention to top-down internally driven representations in a complex motion-processing task. Consistent with the very complex nature of the motion discrimination involved, subjects probably utilize different strategies for deploying their attention, as suggested by the individual differences in motion areas activated. A remaining issue is whether deployment of attention to complex stimuli operates through activation of lower (V3+ and V5/MT+)- or higher-order sensory representations. The pattern of results from this study illustrates that deployment of attention to complex motion activates both higher- and lower-order motion areas, and not lowerorder regions alone. Nine subjects had significant activations in at least one higher and at least one lower-order area, while two subjects had activations only in higher-order areas. No subjects had significant activations in lower-order motion areas alone. Motion stimulus period activity Extensive significant activations in motion-processing regions were observed when we contrasted motion stimulus and fixation

Fig. 3. Examples of cue period motion region activations from individual subject analyses. All activations are significant at P < 0.001, uncorrected from multiple comparisons, and superimposed on SPM2’s canonical single subject T1-weighted image. Abbreviations as for Table 1.

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Table 4 Motion stimulus period group activations in motion-processing regions Comparison of interest

Location Brodmann’s Talairach area coordinates X

Right motion stimuli > fixation

V5/MT+ V3+ VIPS A-SM

Left motion stimuli > fixation

V5/MT+ 37 V3+ 18 VIPS 19 A-SM

Right attended motion > A-SM unattended motion DISPL stimuli Left attended motion > A-SM unattended motion stimuli

37 17 19 39/40

39/7 39/40 7 39/40

Y

t value Z

42 26 24 34 42 32 34 46 38 26 24 32 38 46 46 32

66 77 72 54 53 61 47 48 64 81 72 70 64 45 48 53

8 5.37 11 4.78 30 4.26 36 5.72 38 5.48 29 5.03 26 5.00 54 4.57 5 4.96 11 4.67 37 10.80 44 8.38 50 4.03 34 9.63 52 5.83 62 5.43

42 40 38

40 23 45 22 48 56

6.75 4.38 4.22

All activations are significant at P < 0.001, uncorrected from multiple comparisons. Given coordinates are local maxima >8.0 mm apart within the specified region. Abbreviations as for Table 1.

period activity in a random effects group analysis. In the right attended motion condition, there were significant activations in left V5/MT+, left V3+, left VIPS, left A-SM, and also in right VIPS and right A-SM. In the left-attended motion condition, there were significant activations in left V5/MT+, left V3+, left VIPS, and in right VIPS and right A-SM (Table 4). To investigate the effects of attention and motion discrimination on the activity following motion stimulus presentation, we contrasted the attended and unattended motion stimuli conditions for each visual field. When the attended right motion condition was contrasted with the unattended right motion condition, there were significant activations in left DIPSL and left A-SM. When the attended left motion condition was contrasted with the unattended left motion condition, there were significant activations in left ASM and right A-SM (Table 4). These results are consistent with the visual motion literature; complex motion discrimination tasks activate lower- and higherorder motion areas. The more complex subject of the relationships between brain networks of areas activated during the cue period and the motion stimulus period will be reported in another paper.

Discussion We used fMRI to test the hypothesis that preparatory deployment of attention to motion operates via modulations of higherorder motion-processing areas, even in the absence of relevant external input. To ensure that attentional deployment was purely top-down and not interacting with bottom-up mechanisms, we used a symbolic cue in the absence of any other visual stimuli. This cue was an extremely small increase in the size of the fixation crosshair (so small that it did not create a significant activation in V1 or V2). The cued preparatory deployment of attention, for a complex

motion task, activated higher-order and lower-order motion regions, and not V1 or V2. The motion regions activated included temporal regions consistent with V5/MT+, occipital regions consistent with V3+, SPO, POIPS, ventral, and dorsal IPS, STS, PIC, and A-SM (a region of BA 39/40 superior to V5/MT+ involving the angular gyrus and supramarginal gyrus). These results suggest that anticipatory deployment of attention to internally generated higher-order motion representations operates via top-down modulation of activity in task-relevant processing areas. Consistent with our hypothesis that these motion sensory activations are under top-down control, we found activation of an extensive frontal network following the cue. In addition to the frontal activations (frontal eye field and supplementary eye field) more commonly reported in cued attention studies (e.g., Giesbrecht et al., 2003; Kastner et al., 1999; Shulman et al., 1999), we found activations in anterior cingulate and multiple prefrontal regions. A role for these regions in top-down control of attentional deployment is also supported by models of attentional networks (e.g., Mesulam, 1981; Posner and Peterson, 1990) and recent functional imaging findings. For example, Hopfinger et al. (2000) found dorsal and ventrolateral prefrontal preparatory activations in a cued spatial attention task, and Luks et al. (2002) found anterior cingulate and dorsolateral prefrontal activations associated with preparatory deployment and maintenance of attentional set. The biased competition model of attentional deployment, as proposed by Desimone and Duncan (1995), predicts that preparatory top-down modulation of sensory representations increases the activity of stimulus-selective neurons such that the responses of those neurons to their preferred stimulus, when it appears, are enhanced, and the responses of neurons to competing stimuli are reduced. There is physiological evidence for a bias signal mechanism that enhances lower-level sensory representations (e.g., Kastner et al., 1999; Luck et al., 1997). Here, in the absence of motion stimulation, we have observed activations in locations consistent with lower-level motion-processing regions V5/MT+ and V3+. However, the additional activations we have observed suggest a robust and extensive network of higher-level regions, which probably reflect a more complex preparatory set of processes than can be explained by simple biasing of neurons representing anticipated visual stimuli. The present results suggest that attentional deployment for a complex discrimination task, in the absence of stimulation, involves additional higher-level preparatory mechanisms, and also that these mechanisms (and the cognitive strategies they mediate) may vary across subjects. In particular, several intraparietal sulcus regions were activated in this study. We suggest three explanations for the preparatory activations in these regions, which may be present in any combination within each subject. First, this activation could reflect enhancement of very high-level stimulus representations (e.g., object-from-motion and biological motion processing; Schubotz and Yves von Cramon, 2002; Sunaert et al., 1999). Second, this activation could reflect preparation of the higher-level processing and attention network that will be required for the performance of the motion-processing task (i.e., enhancing of the processing network, including its attention and memory components, rather than enhancing the sensory representations themselves). This would be useful in complex discrimination tasks such as ours, in which the initial encoding of the stimuli may not be the level of processing targeted by preparation, but rather the later-stage motion analysis and perhaps ‘‘object-from-motion’’ processes. Third, these parietal

T.L. Luks, G.V. Simpson / NeuroImage 22 (2004) 1515–1522

activations might reflect aspects of the top-down attentional deployment itself, which, along with frontal and cingulate activations, are mediating the sensory and higher-order preparatory effects in other motion-sensitive regions. Intraparietal sulcus activations have been reported in several cued attention fMRI studies, and have been attributed to the deployment of attention in general, to the deployment of attention in space, and perhaps to the deployment of attention to particular stimulus features, such as motion. (e.g., Corbetta et al., 2000; Friedman-Hill et al., 2003; Hopfinger et al., 2000; Posner and Peterson, 1990; Yantis et al., 2002). Direct comparisons of attentional deployment of different higher-order stimulus features are necessary to identify which effects are feature specific, and which reflect more general processing and attention deployment mechanisms. This is a question not only for IPS regions, but also for all regions of activation, from V5/MT+ to prefrontal cortex. Components of these preparatory processes may overlap with components of other cognitive tasks that rely on similar sensory representation activation and manipulation (such as working memory and mental imagery) or which share higher-level attention and memory components. When attention is deployed to targets that are not present, then top-down biasing and other attentional preparations are likely to activate stored representations of the target features and maintain them during the period of sustained deployment. We expect that this type of attentional deployment would share processes in common with those found in working memory tasks. In addition, in this task, the processes of deploying attention to an internally generated representation of visual stimuli should overlap heavily with the early stages of mental imagery of similar visual stimuli, which must also involve top-down activation of internally generated representations (and also activate V5/MT+ and V3+, e.g., Goebel et al., 1998; Tootell et al., 1995a,b; Zeki et al., 1993). This study included two preparatory attention components; lower-level spatial attention and higher-level motion attention. No significant differences were observed between left and right hemisphere activity when attention was directed to the left vs. right visual field, and there were no significant activations in V1 or V2 following the cue. These results suggest that in this complex motion discrimination task, the initial encoding of the stimuli was not the level of processing targeted by preparatory attention, but rather the later-stage motion analysis and perhaps ‘‘objectfrom-motion’’ processes. The correct spatial location must be attended for accurate performance, but the level of spatial attention required was minimal, relative to the level of attention required to the higher-order motion discrimination performed at that location. It may also be the case that at this higher level, the motion representations and processing components act bilaterally. In those studies that reported spatially specific preparatory attention effects, accurate direction of spatial attention was often the highest level of attentional focus of the experimental design (e.g., O’Connor et al., 2002; Macaluso et al., 2003). Several cued attention studies have also reported primary visual cortex and even lateral geniculate nucleus activation (Kastner et al., 1998, 1999; O’Connor et al., 2003; Ress et al., 2000), while V5/MT+ and V3+ were the lowest levels of significant visual cortex activation observed here. Again, in the present study, attention mechanisms may be acting primarily on the regions representing and processing the higher-order motion feature discrimination, and not the regions responsible for primary visual encoding. This difference in cognitive task may also account for our observation of significant activity in prefrontal and anterior

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cingulate cortex during deployment of attention to top-down internally generated representations, which was not observed in several other cued-attention studies (e.g., Corbetta et al., 2000; Giesbrecht et al., 2003; Kastner et al., 1998, 1999; Macaluso et al., 2003). We observed preparatory attention effects in areas that are well known to respond to motion. Of particular interest, however, was a consistent activation associated with both cues and motion stimuli in a region we have called A-SM, in area BA 39/40 superior to V5/ MT+, involving the angular gyrus and the supramarginal gyrus. This region has not been implicated in basic motion detection by previous fMRI studies that mapped visual motion responses, or by primate electrophysiology studies. Activation in this region was also reported by Shulman et al. (1999) in their cued motion task, but not discussed. We suggest that the relatively consistent activation of this region in the present study is the result of the particular demands of our motion discrimination task. Here, subjects monitored a stream of motion stimuli for a specific target stimulus. While these stimuli varied in multiple motion dimensions (direction of rotation and expansion), the target stimulus may have come to be represented as a ‘‘motion-defined object’’, and thus activated higher-order object processing regions. Perhaps A-SM is one of these object-processing regions. Activations near A-SM have been reported in some fMRI studies of biological motion discrimination, another task that requires higher-order motion-defined object processing (Grossman et al., 2000; Puce et al., 1998). Neville et al. (1998) reported activation close to our A-SM region in response to American Sign Language in both hearing and deaf signers, another example of a complex motion-defined processing task.

Acknowledgments This research was supported by NINDS RO1 NS27900-11, NIMH F32MH64295-01, and NS 45171. We thank Morgan Hough, Corby Dale, Niles Bruce, Evelyn Proctor, and Gary Ciciriello for their assistance with this research.

References Chawla, D., Rees, G., Friston, K.J., 1999. The physiological basis of attention modulation in extrastriate visual cortex. Nat. Neurosci. 2, 671 – 676. Corbetta, M., Kincade, J.M., Ollinger, J.M., McAvoy, M.P., Shulman, G.L., 2000. Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat. Neurosci. 3, 292 – 297. Desimone, R., Duncan, D., 1995. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193 – 222. Driver, J., Frackowiak, R.S.J., 2001. Neurobiological measures of human selective attention. Neuropsychologia 39, 1257 – 1262. Friedman-Hill, S., Robertson, L.C., Desimone, R., Ungerleider, L.G., 2003. Posterior parietal cortex and the filtering of distractors. Proc. Natl. Acad. Sci. U. S. A. 100, 4263 – 4268. Giesbrecht, B., Woldorff, M.G., Song, A.W., Mangun, G.R., 2003. Neural mechanisms of top-down control during spatial feature attention. NeuroImage 19, 496 – 512. Goebel, R., Khorram-Sefat, D., Muckli, L., Hacker, H., Singer, N., 1998. The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery. Eur. J. Neurosci. 10, 1563 – 1573. Grossman, E., Donnelly, M., Price, R., Pickens, D., Morgan, V., Neighbor,

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R.S., Blake, G., 2000. Brain areas involved in perception of biological motion. J. Cogn. Neurosci. 12, 711 – 720. Hopfinger, J.B., Buonocore, M.H., Mangun, G.R., 2000. The neural mechanisms of top-down attentional control. Nat. Neurosci. 3, 284 – 291. Kastner, S., De Weerd, P., Desimone, R., Ungerleider, L.G., 1998. Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. Science 282, 108 – 111. Kastner, S., Pinsk, M.A., De Weerd, P., Desimone, R., Ungerleider, L.G., 1999. Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22, 751 – 761. Kwong, K.K., Belliveau, J.W., Chesler, D.A., Goldberg, I.E., Weisskoff, B.P., Poncelet, R.M., Kennedy, D.N., Hoppel, B.E., Cohen, M.S., Turner, R., Cheng, H., Brady, T.J., Rosen, B.R., 1992. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. U. S. A. 89, 5675 – 5679. Luck, S.J., Chelazzi, L., Hillyard, S.A., Desimone, R., 1997. Neural mechanisms of spatial selective attention in areas of V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77, 24 – 42. Luks, T.L., Simpson, G.V., Feiwell, R.J., Miller, W.L., 2002. Evidence for anterior cingulate cortex involvement in monitoring preparatory attentional set. NeuroImage 17, 792 – 802. Macaluso, E., Eimer, M., Frith, C.D., Driver, J., 2003. Preparatory states in crossmodal spatial attention: spatial specificity and possible control mechanisms. Exp. Brain Res. 149, 62 – 74. Mesulam, M.-M., 1981. A cortical network for directed attention and unilateral neglect. Ann. Neurol. 10, 309 – 325. Neville, H.J., Bavelier, D., Corina, D., Rauschecker, J., Karni, A., Lalwani, A., Braun, A., Clark, V., Jezzard, P., Turner, R., 1998. Cerebral organization for language in deaf and hearing subjects: biological constraints and effects of experience. Proc. Natl. Acad. Sci. 95, 922 – 929. O’Connor, D.H., Fukui, M.M., Pinsk, M.A., Kastner, S., 2003. Attention modulates responses in the human lateral geniculate nucleus. Nat. Neurosci. 5, 1203 – 1209. Ogawa, S., Lee, T.M., Kay, A.R., Tank, D.W., 1990. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. U. S. A. 87, 9868 – 9872. Pessoa, L., Kastner, S., Underleider, L.G., 2003. Neuroimaging studies of attention: from modulation of sensory processing to top-down control. J. Neurosci. 23, 3990 – 3998.

Posner, M.I., Peterson, S.E., 1990. The attention system of the human brain. Annu. Rev. Neurosci. 13, 25 – 42. Puce, A., Allison, T., Bentin, S., Gore, J.C., McCarthy, G., 1998. Temporal cortex activation in humans viewing eye and mouth movements. J. Neurosci. 18, 2188 – 2199. Ress, D., Backus, B.T., Heeger, D.J., 2000. Activity in primary visual cortex predicts performance in a visual detection task. Nat. Neurosci. 3, 940 – 945. Schubotz, R.I., Yves von Cramon, D., 2002. Dynamic patterns make premotor cortex interested in objects: influence of stimulus and task revealed by fMRI. Brain Res. Cogn. Brain Res. 14, 357 – 369. Shulman, G.L., Ollinger, J.M., Akbudak, E., Conturo, T.E., Snyder, A.Z., Petersen, S.E., Corbetta, M., 1999. Areas involved in encoding and applying directional expectations to moving objects. J. Neurosci. 19, 9480 – 9496. Sunaert, S., Van Hecke, P., Marchal, G., Orban, G.A., 1999. Motionresponsive regions of the human brain. Exp. Brain Res. 127, 355 – 370. Tootell, R.B.H., Kwong, K.K., Malach, R., Bom, R.T., Brady, T.J., Rosen, B.R., Belliveau, B.R., 1995a. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neurosci. 17, 7060 – 7078. Tootell, R.B.H., Reppas, J.B., Dale, A.M., Look, R.B., Sereno, M.I., Malach, R., Brady, T.J., Rosen, B.R., 1995b. Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature 375, 139 – 141. Watson, J.D.G., Myers, R., Frackowiak, R.S.J., Hajnal, J.V., Woods, R.P., J.C., Mazziotta, J.C., Shipp, S., Zeki, S., 1993. Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb. Cortex 3, 79 – 94. Yantis, S., Schwarzbach, J., Serences, J.T., Carlson, R.L., Steinmetz, M.A., Pekar, J.J., Steinmetz, M.A., Courtney, S.M., 2002. Transient neural activity in human parietal cortex during spatial attention shifts. Nat. Neurosci. 5, 995 – 1002. Zeki, S., Watson, J.D.G., Lueck, C.J., Friston, K.J., Kennard, C., Frackowiak, R.S.J., 1991. A direct demonstration of functional specialization in human visual cortex. J. Neurosci. 11, 641 – 649. Zeki, S., Watson, J.D., Frackowiak, R.S., 1993. Going beyond the information given: the relation of illusory visual motion to brain activity. Proc. R. Soc. Lond. B., Biol. Sci. 252, 215 – 222.