Elsevier

NeuroImage

Volume 18, Issue 3, March 2003, Pages 633-641
NeuroImage

Regular article
The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention

https://doi.org/10.1016/S1053-8119(02)00012-5Get rights and content

Abstract

The purpose of this study was to identify brain regions underlying internally generated anticipatory biases toward locations where significant events are expected to occur. Subjects fixated centrally and responded to peripheral targets preceded by a spatially valid (predictive), invalid (misleading), or neutral central cue while undergoing fMRI scanning. In some validly cued trials, reaction time was significantly shorter than in trials with neutral cues, indicating that the cue had successfully induced a spatial redistribution of motivational valence, manifested as expectancy. The largest cue benefits led to selectively greater activations within the posterior cingulate and medial prefrontal cortex. These two areas thus appear to establish a neural interface between attention and motivation. An inverse relationship to cue benefit was seen in the parietal cortex, suggesting that spatial expectancy may entail the inhibition of attention-related areas to reduce distractibility by events at irrelevant locations.

Introduction

Visual spatial attention allows us to allocate neural processing resources to those parts of the visual environment that have relevance to ongoing behavior. There is now significant evidence that this ability is mediated through a monosynaptically interconnected network including regions of the frontal, parietal, and cingulate cortex Andersen 1990, Barbas and Mesulam 1981, Corbetta et al 1993, Gitelman et al 1999, Kim et al 1999, Koski et al 1998, Mesulam 1999, Mesulam et al 1977, Nobre et al 1997, Stanton et al 1993, Stanton et al 1995. Clinical support for this formulation comes from the observation that damage to any of these three components can lead to a state of contralesional inattention known as hemispatial neglect. Single unit recordings in macaques and functional imaging in humans have helped to delineate the differential specializations of the parietal and frontal components of this network for perceptual representation, sensory–motor transformation, target search, stimulus detection, fixation, encoding of salience, focusing, and attentional shifting Andersen 1995, Bushnell et al 1981, Corbetta et al 2000, Gitelman et al 1996, Goldberg and Bushnell 1981, Hopfinger et al 2000, Mesulam 1999, Pare and Wurtz 1997, Robinson et al 1995, Rushworth et al 2001, Segraves and Goldberg 1987, Snyder et al 1998, Vandenberghe 2001. The role of the cingulate gyrus in spatial attention has been more difficult to specify.

The cingulate region has a complex neuroanatomy and displays regional variations in its attention-related affiliations. Numerous functional imaging studies, for example, have reported activations in the anterior cingulate region (often extending into the supplementary motor area) during tasks of visual search, manual exploration, target detection, and covert shifts of attention Corbetta et al 2000, Gitelman et al 1996, Gitelman et al 1999, Hopfinger et al 2000, Kim et al 1999, Nobre et al 1997, Nobre et al 2000b. The anterior cingulate cortex has also been implicated in additional tasks of potential relevance to spatial attention such as spatial working memory, selection-for-action, conflict monitoring, and vigilance Botvinick et al 1999, Carter et al 2000, MacDonald et al 2000, Naito et al 2000, Nobre et al 2000a, O’Sullivan et al 1995, Paus et al 1993, Petit et al 1996.

The posterior cingulate region seems to have a different set of attention-related affiliations. In the macaque, neurons of the posterior cingulate gyrus fire tonically during steady gaze at a rate determined by the direction of the preceding eye movement and the current angle of the eye in the orbit (Olson et al., 1996). Their activity increases immediately following saccadic eye movements. Saccadic eye movements to the same target can elicit different firing intensities if they are based on contraversive versus ipsiversive saccades. These neurons therefore seem to be encoding the direction of displacement rather than the location of the target. Since their activity is postsaccadic, they are likely to be monitoring rather than controlling shifts of visual attention. Alternatively, these neurons could be encoding a postsaccadic resetting of the attentional map in anticipation of the next attentional shift.

The cingulate gyrus is part of the paralimbic belt and is heavily interconnected with structures such as the orbitofrontal cortex and amygdala Mesulam et al 1977, Morecraft et al 1992, areas known to be important in regulating motivation. Although these anatomical relationships had led to the conjecture that the cingulate region may mediate the motivational guidance of spatial attention (Mesulam et al., 2001), experimental support for this formulation has been difficult to obtain. In a previous block-design fMRI study we showed that covert shifts of visual spatial attention led to the activation of two cingulate foci, one in the posterior cingulate cortex (PC) and the other in the anterior cingulate cortex (AC). However, only the PC activation was correlated with the speed of detecting a lateralized visual target in a task where targets were preceded by a predictive cue (Mesulam et al., 2001). These results led us to hypothesize that the AC and PC make different contributions to visual spatial attention and that the PC may selectively mediate emergence of cue-induced visuospatial expectancy, a process that entails the redistribution of motivational relevance within the extrapersonal space. Circumstantial support for this hypothesis is provided by the finding that the PC is more sensitive to cues than to targets in attention-shifting tasks where spatially predictive cues precede targets (Hopfinger et al., 2000).

The current study was specifically designed to test this hypothesis. We used event-related fMRI to isolate single trials in which evidence for an anticipatory visual bias could be established. A variation of the Posner paradigm was used (Posner, 1980) (Fig. 1). Subjects fixated on the center of a screen and responded to peripheral targets, displaced at either side of a central diamond. Targets were preceded by changes in the central diamond that provided a spatially valid (predictive), invalid (misleading), or neutral (nondirectional) cue. We reasoned that if the PC facilitates spatial shifts of expectancy, its activity should be greatest in trials where spatially informative cues could be shown to have accelerated target detection, indicating that an anticipatory bias in the direction of the cue had been established.

Section snippets

Subjects

The Institutional Review Board at Northwestern University approved the study protocol. Fifteen healthy volunteers (6 men and 9 women) with a mean age of 26 years gave written informed consent and participated in two sessions. During the first session, subjects completed the psychophysical task in a laboratory setting. This session was necessary to familiarize subjects with the task and to ensure that they were able to maintain fixation. In the second session subjects completed the task during

Behavioral data

Analysis of the eye data indicated that subjects had no difficulty maintaining fixation throughout the experiment. On average 1.2 saccades were made during each run with the mode number saccades at 0 and the maximum number of saccades during any one run being 6.

Accuracy of target detection was above 90% in all sessions. The mean accuracy for the ND trials was 99.1% (SD = 0.7%), for the valid trials 99.3% (SD = 0.7%), and for the invalid trials 99.1% (SD = 1.5%). A within-subjects

Discussion

A fundamental purpose of the spatial attention system is to expedite target detection at locations where significant events are expected to occur. The internal generation of this “expectancy” entails a spatial redistribution of motivational relevance. Results obtained in a previous study had led us to propose that this aspect of spatial attention might be mediated by the posterior cingulate cortex Kim et al 1999, Mesulam et al 2001. In support of our hypothesis, the present experiments showed

Conclusion

The cingulate gyrus had been identified as a major cortical component of a distributed network subserving the dynamic reallocation of spatial attention Mesulam 1981, Mesulam et al 2001. In keeping with this formulation, previous studies have shown that the anterior cingulate gyrus is activated in numerous tasks of spatial attention, including target detection. The use of an event-related design in the current study allowed us to show that the posterior cingulate gyrus is also part of this

Acknowledgements

This work was supported by the NIA (Grant K23 AG00940-02) awarded to D.R. Gitelman, Northwestern Alzheimer’s Disease Center (Grant PHS AG138541) awarded to D.M. Small, and NINDS (Grant NS30863-03) awarded to M-M. Mesulam. We thank our research assistants Suzanne Bloise, Kensan Lam, and Ramesh Srinivasan for all their help.

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