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

Key Points

  • This review proposes that two networks of brain areas are involved in controlling attention. One network is primarily responsible for applying cognitive, top-down selection for stimuli and responses, whereas the other detects behaviourally relevant stimuli and might act as a 'circuit breaker' for the first system.

  • Humans use cognitive information to direct attention to relevant objects (targets) in a visual scene. Information such as the target's colour or location is represented as a 'perceptual set'. Similarly, advance information about the required response to a target is represented as a 'motor set'. These can be considered together as an 'attentional set', which aids the detection of and response to targets.

  • Such top-down control of attentional processes activates dorsal posterior parietal and frontal regions of the brain bilaterally in both monkeys and humans. This dorsal frontoparietal system is responsible for the generation of attentional sets.

  • Attention can also be driven by stimulus properties rather than cognitive processes. This 'bottom-up' control of attention explains why we find ourselves drawn to 'oddball' stimuli that are very different from the background, or to salient stimuli that share some sensory features, such as colour, with the target for which we are searching. The dorsal frontoparietal system seems to maintain a 'salience map' that combines bottom-up with top-down information during visual search.

  • Potentially important sensory stimuli, such as loud alarms or sudden movement, can attract our attention regardless of the ongoing task. This sensory orienting process seems to be mediated by the second attentional network, which is mainly lateralized to the right side of the brain and includes the temporoparietal junction and the ventral frontal cortex. This network seems to interrupt ongoing cognitive activity when a stimulus that might be behaviourally important is detected.

  • These two networks could interact in humans to control attention. It is possible that damage to these networks is responsible for the syndrome of neglect, in which patients that have suffered damage to the right side of the brain tend to ignore stimuli on the left side of space. The authors suggest that neglect results from damage to the ventral network that also 'functionally inactivates' the dorsal network.

Abstract

We review evidence for partially segregated networks of brain areas that carry out different attentional functions. One system, which includes parts of the intraparietal cortex and superior frontal cortex, is involved in preparing and applying goal-directed (top-down) selection for stimuli and responses. This system is also modulated by the detection of stimuli. The other system, which includes the temporoparietal cortex and inferior frontal cortex, and is largely lateralized to the right hemisphere, is not involved in top-down selection. Instead, this system is specialized for the detection of behaviourally relevant stimuli, particularly when they are salient or unexpected. This ventral frontoparietal network works as a 'circuit breaker' for the dorsal system, directing attention to salient events. Both attentional systems interact during normal vision, and both are disrupted in unilateral spatial neglect.

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Figure 1: The Garden of Earthly Delights by Hieronymous Bosch.
Figure 2: Dorsal frontoparietal network for top-down control of visual attention.
Figure 3: Overlap between working memory and attention.
Figure 4: Dorsal frontoparietal network during response selection and stimulus–response mapping.
Figure 5: Dorsal frontoparietal network and salience.
Figure 6: Ventral right frontoparietal network and target detection.
Figure 7: Neuroanatomical model of attentional control.

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Acknowledgements

This work was supported by the National Institutes of Health and The J. S. McDonnell Foundation. We thank M. Kincade, A. Tansy, M. Linenweber, S. Astafiev and G. d'Avossa for scientific collaboration; M. Cowan for figure preparation; C. Stanley for scanning; and L. Snyder for contributing data to figure 4a.

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Correspondence to Maurizio Corbetta.

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FURTHER INFORMATION

brain imaging: localization of brain functions

brain imaging: observing ongoing neural activity

magnetic resonance imaging

 MIT Encyclopedia of Cognitive Sciences

attention

attention in the human brain

eye movements and visual attention

James, William

magnetic resonance imaging

positron emission tomography

top-down processing in vision

visual neglect

working memory

Glossary

TOP-DOWN PROCESSING

The flow of information from 'higher' to 'lower' centres, conveying knowledge derived from previous experience rather than sensory stimulation.

BOTTOM-UP PROCESSING

Information processing that proceeds in a single direction from sensory input, through perceptual analysis, towards motor output, without involving feedback information flowing backwards from 'higher' centres to 'lower' centres.

FRONTAL EYE FIELD

An area in the frontal lobe that receives visual inputs and produces movements of the eye.

SACCADIC EYE MOVEMENT

A rapid eye movement that brings the point of maximal visual acuity — the fovea — to the image of interest.

NEGLECT

A neurological syndrome (often involving damage to the right parietal cortex) in which patients show a marked deficit in the ability to detect or respond to information in the contralesional field.

LOCUS COERULEUS

A nucleus of the brainstem. The main supplier of noradrenaline to the brain.

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Corbetta, M., Shulman, G. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3, 201–215 (2002). https://doi.org/10.1038/nrn755

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