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vation was close to that found by a different group when purely chromatic stimuli were passively viewed [3--l. Similarly, focal attention to motion activated a midtemporal area that was close to areas activated by passive visual motion and visual pursuit [2--,3-l.

Recent advances in neuroimaging of human brain activity, particularly positron emission tomography (PET), have facilitated explorations of the anatomy of attention. Many PET studies compare active conditions, where subjects attend to stimuli in order to perform a particular task, with conditions where subjects passively receive the same stimuli. Such comparisons reveal the specific brain areas involved in attention. (For a review of the anatomical basis of human attention, see [l] .> Recently, PET studies have been related to electrical recordings of neural activity in both humans and animals allowing explorations of the ordering of these anatomical activations. These methodological developments will be reviewed in the context of four main areas of selective attention research.

One limitation of the current PET methods is that they require averaging of responses over extended periods of time. Electrical recordings from the scalp, trace the time-course of activation in more detail, and thus allow closer analysis of the ordering of the anatomical activations found with PET. Can scalp recording detect sufficiently localized changes? While some algorithms for localizing generators have appeared [4,5-,6], it remains unclear how they will cope with several concurrent generators, which seem likely for most cognitive tasks. One approach to this problem is to examine whether localization of scalp activity converges with the areas activated in blood flow studies. When visual attention is manipulated by spatial cueing during color judgements, currentsource density analysis shows amplification of activity over a prestriate region close to that found in PET studies of color processing [ 3**,6]. The amplification is apparent at about 100 ms, demonstrating attentional modulation of relatively early coding. Consistent with an early perceptual effect, recent behavioral studies confmn that visual attention to a retinal location improves sensitivity for events at the attended location [ 71. Electrical and magnetic recordings have also revealed attentional amplifications in audition [WI. While the auditory amplifications appear to be sensory, as responses are modulated in areas close to primary auditory cortex, they tend to involve the addition of new electrical sources rather than a simple increase in the existing electrical responses.

Amplification Studies of brain metabolism, electrical activity, and magnetic activity have revealed that attention produces a relative enhancement of task-relevant signals within sensory specific cortical systems. Particularly noteworthy, is a human PET study in which focal attention to changes in color, form and motion were compared with passive viewing of the same displays, and with divided attention when all three types of change had to be detected [2*-l. Relative to divided attention, the focal attention conditions activated prestriate regions which are likely candidates for visual areas specializing in the attended attribute. In the case of color, one area of enhanced acti-

Abbreviation PET-positron @ Current

emission tomography.

Biology

Ltd ISSN 0959-4388

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Cognitive neuroscience

Sources of attention:

networks

and nodes

How do these results relate to recordings of individual cells during attentional tasks? The review began by describing attentional amplification of metabolic and electncal activity in prestriate areas. Studies that have recorded from individual neural cells in alert monkeys within prestriate areas [9] show inhibition of firing rates to an optimal stimulus placed within their receptive field when attention is directed to a less optimal stimulus, within the same receptive field. In this case, selection appears to work more by inhibiting responses at unselected locations rather than amplification of the selected location. In other cases, however, there is evidence of increased firing rates in prestriate areas with attention to a stimulus [9]. A recent review of many studies of attention in alert monkeys [lo**] shows selective enhancement of firing rates of cells in the parietal lobe and other areas when attention is directed to stimuli in their receptive field. In considering these data, it is important to distinguish the sites of observed visual attention modulations (e.g. prestriate cortex) from the potential sources of such modulation (e.g. parietal frontal cortex). The PET study that revealed prestriate amplification [2-l also found activation of anterior cingulate gyrus, several sites in the basal ganglia, and right lateral frontal cortex, when divided and focal attention conditions were compared with passive viewing. These additional activations presumably reflect sources of the prestriate amplifications. Further PET studies have revealed several networks of inter-linked areas which appear to be the sources for various kinds of attentional modulation. It has been proposed [l] that a network of anatomical areas involving the parietal lobe performs the function of covert orienting to visual locations, while more anterior network involving the basal ganglia and anterior cingulate gyrus is concerned with the process of detecting targets and preparing appropriate responses. The evidence for a source of attention effects is most complete for orienting to visual locations. A recent PET study (M Corbetta et al: J Blood Flow Metab [Abstrj 1991, 11:909), still to be published in full, has compared the passive presentation of a series of stimuli in one visual field, with a condition where subjects had to shift attention to successive locations within a visual field to detect the targets. The latter condition produced activation in the superior parietal lobe as well as the frontal cortex. Within a visual field, the direction of attentional shifts made no difference to the observed activation. Shifts of attention in the left visual field activated the right parietal lobe, whereas right visual field shifts activated both panetal lobes. These data suggest that the right parietal lobe is involved in attention shifts for both visual fields, while the left lobe deals only with the contralateral side. This might explain the clinical finding that patients with right parietal lesions usually have more profound attentional deficits than those with left parietal lesions. There is some evidence that the computations involved in spatial visual orienting are distributed within a network of anatomical areas that include the cortex (parietal area),

thalamus (lateral pulvinar), and midbrain (superior colliculus). Each of these anatomical areas (nodes) is in volved in shifts of visual attention, but each node may perform a different operation. A recent behavioral study has suggested that the superior colliculus is important in covert shifting of visual attention [ 11] , while a PET study has confirmed the hypothesized involvement of the pulvinar nucleus in filtering out information from irrelevant locations [ 121. According to one model [ 121, the parietal lobe is involved in establishing expectations of target location, while the pulvinar performs a filtering operation to exclude information from elsewhere. Data from alert monkey studies, involving lesions and cellular recording from these same areas, confirm their involvement in selective attention. They also suggest that the changes found in prestriate cortex are imposed from elsewhere, but have not yet shown evidence of differentiation among the parietal lobe, pulvinar and superior colliculus areas in the operations they are performing [9,10-*I. There is evidence from PET work that a different, modality-independent attentional network is involved in maintaining vigilance [ 13*]. Subjects who had to sustain attention to vision or somatosensory information in order to detect very rare signals, showed activation in a cluster of right frontal and parietal areas. These results confirm earlier suggestions that right hemisphere regions are cru cial for maintaining an alert state [ 11. A number of PET studies have implicated a third attentional network, involving the anterior cingulate gyrus, in the detection of multiple targets [ 11 and inhibition of dominant responses [14]. The processing of pain can now be added to the growing list of cingulate functions. A recent study [ 15.1 applied heat to the fingertips, and compared the amount of activation for intensities that did or did not produce pain. The anterior cingulate gyrus was the most prominent area activated by pain, One problem with the cingulate gyrus functions proposed on the basis of PET data is that stereotaxic lesions to this area for intractable pain and depression have not produced the severe cognitive deficits that would be expected. A recent paper, however, suggests that such lesions produce deficits in just the type of tasks that have been found to activate the area in PET studies [ 161. These deficits are transient, suggesting that the anterior cingulate gyrus is not a unique source of higher-level attentional control.

Visual

search

What are the consequences of the amplifications found in blood flow and electrical activity within prestriate areas? As noted above, visual attention to a location improves the ability to detect targets there, but can a more precise characterization of the computations affected by attention be provided? Searching for a specified visual target among a varied number of non-targets has been widely used to examine this issue. Although eye movements often take place during search, shifts of visual attention can occur without any eye movement. These covert attention shifts improve sensitivity to areas outside the fovea. Atten-

The neurobiology

tion shifts appear to precede the eye movement and are a method of selecting areas of the visual field that will be foveated next. Even within a single fixation several shifts of covert attention may occur. One recent estimate suggests that covert shifts of visual attention can be as rapid as 30-50 ms [ 171, which would allow several regions to be searched within a single fixation. Visual search experiments have shown that the time required to detect a target defined by a unique feature (e.g. the only red item) is unaffected by the number of non-targets. Search for a target defined by a conjunction of features (e.g. a red square among blue squares and red circles) has been found to increase linearly with the number of non-targets. This prompted the idea that attention is required for the appropriate combining of visual attributes, thought to be computed by distinct prestriate areas [IS], into an object having these features. It is as though conjoining features into an object requires attention to each location in turn. While it remains clear that some searches require serial attention and others do not, the feature conjunction hypothesis has come under considerable scrutiny, with several reported cases of conjunction search not being affected by the number of nontargets [ 19,201. As a result, the theory has been modified [21,22*-l. According to this modified view, search may be based upon dimensions other than spatial location. For example, one can search for a red square by restricting search only to those items that are red, and looking only among them for a particular form. The incorporation of the ability to select by color or motion into the theory is consistent with the neuroimaging data discussed earlier showing attentional amplification when looking for targets deftned by these dimensions. Searching for targets defined by the absence of a feature (e.g. 0 among Q’s) appears to require serial attention. The reaction times for detecting an 0 increase linearly with the number of distracting Q’s [I8]. The difference between feature-present and feature-absent search has been used to examine what properties the visual systern considers as features [22**]. Some of the attributes turn out to be surprisingly sophisticated (e.g. three-dimensional orientation derived from two-dimensional pictorial cues) [23]. The same attributes (e.g. tilt) appear to be coded as features regardless of the media (luminance, texture, depth, color, or motion) in which the stimuli are defined [24]. When compared with featurepresent tasks, feature-absent search produces characteristic electrical activity that is maximal at electrode sites above the parietal cortex [ 251. This suggests the presence of increased neural activity in parietal cortex during the more serial, feature-absent search. Control of serial visual search by the cortex is also suggested by a comparison of normal subjects and patients whose two hemispheres had been surgically disconnected. Normal subjects show the same linear increase in reaction time when searching for a conjunction target, whether the stimuli are all placed within one visual field or are separated between the two visual fields. Unlike normal subjects, the split-brain pa tients could search independently and concurrently in

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each visual field during a conjunction-search task, with the result that they scanned bilateral arrays faster [26]. Parietal cortex is implicated in the feature-conjunction process by data from a patient with unilateral damage to this area. This patient made many feature miscombinations when reporting contralateral colored shapes, but could accurately report the individual features on the affected side [27-l.

Attention

and mental representation

The effects of attention on the performance of normal subjects can reveal the nature of the mental representa tions that are selectively amplified. Sever+ recent studies have demonstrated attentional modulation_of .perceptual after-effects considered to reflect/early perceptual processes. In the motion aftereffect, extended viewing of a moving stimulus induces a sensation of opposite motion in subsequent stationary or ambiguous test stimuli. This effect is attenuated if the adapting stimulus is unattended [28,29]. Attentional deficits following brain damage provide further information about the mental representations on which attention can operate. Unilateral ablation of the frontal eye field (area 8) in primates produces transient neglect for distant, but not near, contralateral objects. The converse attentional deficit is observed following unilateral damage to frontal area 6 [30]. This suggests that the representations for near and far space may be distinct, at least in monkeys [31]. A similar distinction may apply to the representation of space in the human brain, as left neglect for near, but not for far, space has recently been observed in a patient following right middle cerebral artery infarction [32]. Attentional deficits affecting particuiar representations can also be observed when a subject is reading, as two recent collections of work on neglect dyslexia attest [33,34]. Patients with neglect dyslexia following unilateral brain injury omit or mis-identify letters at the contralateral end of printed strings, despite having no visual field defects. This problem can apparently arise at a number of diIferent representational levels. In the majority of reported cases, errors arise for letters on the side contralateral to the patient’s lesion. One patient with a left-hemisphere lesion, however, made errors for letters towards the end of words regardless of whether these were presented in conventional left-to-right format, vertically, or in mirror-image format, such that the final letters were now on the patient’s left rather than right [35]. This suggests that letter-strings can be mentally represented in abstract word-centered coordinates, Such phenomena are not restricted to reading. A patient with a right-hemisphere lesion has been found to show object-centered neglect in shape perception, such that details on the left of elongated nonsense shapes are ignored even when the shape is tilted 45”~ that some of these details fall to the patient’s right [36].

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Perspective The apparent fractionation of neglect into attentional deficits at distinct levels of representation has suggested to some authors that attentional mechanisms cannot be distinguished from the representational systems in which selectivity arises. It remains to be seen how this view can be reconciled with the evidence discussed earlier suggesting that the sources of attention can be distinguished from the sites of the resulting attentional modulation. Proceedings of a recent conference [37] illustrate the theoretical tension between those who consider attentional operations to be highly task-specific (for an example, see [38]) and those proposing general purpose selective networks (for examples, see [ 1,391). Whichever view prevails, it is clear that many anatomical areas are involved in selective attention.

6.

Mangun GR, HilIyard SA: Electrophysiological Studies of Viof sual Selective Attention in Humans. In Neurobiology Higher Cognitive Function. Edited by Scheibel AB, Wechsler AF. New York: Guildford Press; 1990: 271-294.

7.

HAWKINS HL, HILLYARDSA, LUCK SJ, MOUIOUA M, DOWNING CJ, WOODWARD DP: Visual Attention Modulates Signal De-

tectability.

J Eq

Psych1 [Hum

8. ..

NAATANEN R: The

9.

DESIMONE R, WESXNER

tion and Sci This paper trates how tention.

Percept]

1990, 16:802+311.

Role of Attention in Auditory InformaProcessing as Revealed by Event-Related Potentials Other Measures of Cognitive Function. Behav Brain 1990, 13: 201-288. reviews studies of attention to auditoty stimulation. It illussuch information leads to a theory of auditory selective at-

M, THOMAS L, SCHNEIDERW: Attentional Control of Visual Perception: Cortical and SubcorticaI Mechanisms. Cold Spring Harb Symp Quant Biol 1992, in press.

10.

COLBY CL: The Neuroanatomy and Neurophysiology tention. J Child New-01 1991, 6:S90-S118. %s is an excellent review of the cellular recording approach tive attention.

Acknowledgements Research for the paper was supported by the Ofice of Naval Re search Contract NOOO14-89~3013, the Pew Memorial Trusts and James S McDonnell Foundation support of the Center for Cognitive Neuroscience of Attention.

of Atto selec-

11.

SPRAG~JE JM: The Role of the Superior CoIIicuIus in FaciIitating Visual Attention and Form Perception. Proc Nat1 Acad Sci USA 1991, 88:12861290.

12.

IAE~ERCED: ThaIamic

and Cortical Mechanisms of Attention Suggested by Recent Positron Emission Tomographic Experiments. J Cog Neurosci 1990, 2:35%372.

of a Human System PARW J, Fox P, RAICHLEM: Localization for Sustained Attention by Positron Emission Tomography. Nature 1991, 349:61X% Right frontal and parietal areas are found to be active during sustained attention regardless of sensory modality. 13. .

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