A functional MRI study of preparatory signals for spatial location and objects

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Abstract

We investigated preparatory signals for spatial location and objects in normal observers using functional magnetic resonance imaging (fMRI). Activity for attention-directing cues was separated from activity for subsequent test arrays containing the target stimulus. Subjects were more accurate in discriminating a target face among distracters when they knew in advance its location (spatial directional cue), as compared to when the target could randomly appear at one of two locations (spatial neutral cue), indicating that the spatial cue was used. Spatially specific activations occurred in a region at the intersection of the ventral intraparietal sulcus and transverse occipital sulcus (vIPS-TOS), which showed significantly stronger activation for rightward- than leftward-directing cues, while other fronto-parietal areas were activated by the cue but did not show spatial specificity. In visual cortex, activity was weak or absent in retinotopic occipital regions following attention-directing cues and this activity was not spatially specific.

In a separate task, subject discriminated a target outdoor scene among distracters after the presentation of spatial neutral cues. There was no significant difference in dorsal frontoparietal activity during the face versus scene discrimination task. Also, there was only weak evidence for selective preparatory activity in ventral object-selective regions, although the activation of these regions to the subsequent test array did depend upon which discrimination (face or place) was performed. We conclude first that under certain circumstances, spatial cues that produce strong behavioral effects may modulate parietal-occipital regions in a spatially specific manner without producing similar modulations in retinotopic occipital regions. Second, attentional modulations of object-selective regions in temporal-occipital cortex can occur even though preparatory object-selective modulations of those regions are absent or weak.

Introduction

When looking at a visual scene, we can focus attention on the location or the identity/features of objects (e.g. whether it is a face or a building), and both forms of selection may occur during normal vision. A growing number of brain imaging studies have implicated a set of dorsal frontoparietal areas, including the putative human homologues of monkey areas LIP and FEF in the control of visual attention (reviewed in Corbetta & Shulman, 2002; Kanwisher & Wojciulik, 2000; Pessoa, Kastner, & Ungerleider, 2003). Activity in these areas is time-locked to the onset of cue stimuli that instruct subjects to direct and maintain attention to a location, or switch attention between locations, features, or whole objects (Corbetta, Kincade, Ollinger, McAvoy, & Shulman, 2000; Hopfinger, Buonocore, & Mangun, 2000; Kastner, Pinsk, De Weerd, Desimone, & Ungerleider, 1999; Liu, Slotnick, Serences, & Yantis, 2003; Shulman et al., 1999, Yantis et al., 2002). It has been proposed that these areas selectively bias visual cortex so that it responds more strongly to behaviorally relevant objects. For example, when expecting a certain object at a certain location, dorsal frontoparietal areas may bias activity, prior to stimulus presentation, in visual areas that code for the attended location and object.

Although studies indicate that preparatory signals in some dorsal areas do code selectively for attended visual attributes (e.g. location, direction of motion) (Bisley & Goldberg, 2003; Corbetta, Kincade, & Shulman, 2002; Hopfinger et al., 2000; Shulman, D’Avossa, Tansy, & Corbetta, 2002), the presence of selective activity is usually accompanied by a much more widespread activation of posterior parietal and frontal cortex, which appears to be general and not selective. The generality of frontoparietal recruitment during visual attention tasks has led to the proposal that activity in this network correlates with general factors such as perceptual difficulty or load (Marois, Chun, & Gore, 2000; Wojciulik & Kanwisher, 1999). Therefore, one goal of this experiment was to test the specificity of preparatory signals in dorsal fronto-parietal regions for location, by asking subjects to covertly attend to either a left or right visual field location.

Dorsal fronto-parietal areas are thought to control and modulate the inflow of visual sensory information from particular locations by sending biasing signals to regions in occipital cortex. In support of this idea, Kastner et al. reported a positive change of the blood oxygenation level dependent (BOLD) signal in visual cortex (both striate and extrastriate) prior to the presentation of a test array, consisting of complex visual pictures, at an expected location (Kastner et al., 1999). This expectation-related signal increase, known as a baseline signal, appeared to be location-selective since it was only seen in retinotopically appropriate regions of visual cortex (see also Hopfinger et al., 2000; Ress, Backus, & Heeger, 2000). However, in an experiment in which the location of a stimulus was cued, we failed to observe baseline shifts in visual cortex that varied with the direction of the cue, even though we observed behavioral effects of the cue as well as cue-related modulations in dorsal fronto-parietal regions (Corbetta et al., 2000). These results raise the question of whether behaviorally effective cues that modulate parietal cortex necessarily produce preparatory spatially specific biasing signals in retinotopic visual cortex.

Therefore, a second goal of the experiment was to revisit the issue of spatially-specific baseline signals in retinotopic visual cortex using a paradigm that was more similar to Kastner et al. (e.g. a match-to-sample task involving complex objects) while providing additional controls for the distribution of attention in the visual field. If baseline signals in retinotopic regions of visual cortex are location-specific, then they should move with the attended visual location. Since Kastner et al. cued the same location on each trial, they were not able to test this prediction.

While previous studies of attention have examined the specificity of dorsal fronto-parietal areas for simple features such as location or motion direction, less work has been directed at more complex classes of objects. Studies have indicated that regions in fusiform (‘fusiform face area’, FFA (Kanwisher, McDermott, & Chun, 1997)) and parahippocampal (‘parahippocampal place area’, PPA (Epstein & Kanwisher, 1998)) cortex show selective sensory-evoked responses to faces and places, respectively. Moreover, responses in FFA are modulated according to whether the task requires face or place discriminations (Wojciulik, Kanwisher, & Driver, 1998). If preparatory signals in the dorsal network also reflect object coding, then the spatial distribution or magnitude of preparatory activity may vary with the type of object. Conversely, if the dorsal network is primarily involved in selecting the location of objects, then similar preparatory signals should occur when either a face or an outdoor scene is expected. Therefore, a third goal of the experiment was to test for the specificity of biasing signals in dorsal fronto-parietal regions for different classes of objects, by asking subjects to perform object recognition tasks using unfamiliar faces or outdoor scenes.

Finally, task-specific modulations in FFA and PPA to faces and houses may result from preparatory biasing signals in fusiform cortex, analogous to the spatial biasing signals observed in retinotopic cortex. Therefore, a fourth goal was to examine whether selective, preparatory biasing signals could be observed in object-specific extrastriate regions. By cueing specific types of objects at particular spatial locations, we tested whether preparatory baseline shifts occur both in early retinotopic areas that process information presented at the cued location and in higher-order extrastriate regions that generalize over location but selectively process the object-type (e.g. face versus house) that has been cued.

Section snippets

Subjects

Twenty-one subjects were recruited from the Washington University community for experiment 1. Four subjects, all of whom had participated in experiment 1, participated in experiment 2. Informed consent was obtained in accordance with procedures approved by the local human studies committee. All subjects were strongly right-handed as measured by the Edinburgh Handedness Inventory, had normal or corrected-to-normal vision, and normal neurological history.

Apparatus and stimuli

Stimuli were projected using an Epson

Behavioral performance

Accuracy and RT data were analyzed with a 2 × 2 within-subject ANOVA with spatial cueing (face directional, face neutral), and discrimination (match, no-match) as factors. Responses were averaged across locations since no significant differences were found in accuracy or reaction times (RTs) between the two fields. Subjects used the spatial cue to solve the task. They were more accurate and faster in the face discrimination task when the arrow cue pointed to one location (directional cue) than

Visual field selectivity of preparatory signals for spatial attention in parietal regions

A rather puzzling observation, replicated now several times, is that preparatory signals in dorsal frontoparietal areas for spatial attention show weak evidence of location-selectivity during tasks that force subjects to either maintain covert attention on a location or switch attention between locations (e.g. Corbetta et al., 2000, Yantis et al., 2002). This result is puzzling since one would expect spatial attention signals to operate within a spatial map coding for extrapersonal locations,

Acknowledgements

MH71920-06, and the J.S. McDonnell Foundation.

References (53)

  • M.C. Bushnell et al.

    Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention

    Journal of Neurophysiology

    (1981)
  • J.L. Calton et al.

    Non-spatial, motor-specific activation in posterior parietal cortex

    Nature Neuroscience

    (2002)
  • D. Chawla et al.

    The physiological basis of attentional modulation in extrastriate visual areas

    Nature Neuroscience

    (1999)
  • C.L. Colby et al.

    Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area

    Journal of Neurophysiology

    (1996)
  • J.D. Connolly et al.

    Human fMRI evidence for the neural correlates of preparatory set

    Nature Neuroscience

    (2002)
  • M. Corbetta et al.

    Voluntary orienting is dissociated from target detection in human posterior parietal cortex

    Nature Neuroscience

    (2000)
  • M. Corbetta et al.

    Neural systems for visual orienting and their relationship with working memory

    Journal of Cognitive Neuroscience

    (2002)
  • M. Corbetta et al.

    A PET study of visuospatial attention

    Journal of Neuroscience

    (1993)
  • M. Corbetta et al.

    Control of goal-directed and stimulus-driven attention in the brain

    Nature Reviews. Neuroscience

    (2002)
  • S.M. Courtney et al.

    Transient and sustained activity in a distributed neural system for human working memory

    Nature

    (1997)
  • E. DeYoe et al.

    Mapping striate and extrastriate visual areas in human cerebral cortex

    Proceedings of the National Academy of Sciences of the United States of America

    (1996)
  • R. Epstein et al.

    A cortical representation of the local visual environment

    Nature

    (1998)
  • N. Hadjikhani et al.

    Retinotopy and color sensitivity in human visual cortical area V8

    Nature Neuroscience

    (1998)
  • K.M. Heilman et al.

    Attention: Behaviour and neural mechanisms

  • J.B. Hopfinger et al.

    The neural mechanisms of top-down attentional control

    Nature Neuroscience

    (2000)
  • S. Kakei et al.

    Direction of action is represented in the ventral premotor cortex

    Nature Neuroscience

    (2001)
  • Cited by (0)

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