- Email: [email protected]
A framework for studying the neural basis of attention
Neuropsychologia 39 (2001) 1367– 1371 www.elsevier.com/locate/neuropsychologia
Concluding review
A framework for studying the neural basis of attention Chris Frith * Wellcome Department of Cogniti6e Neurology, Institute of Neurology, Uni6ersity College London, 12 Queen Square, London WC1N 3BG, UK
Abstract There is a high degree of consensus between the contributors to this volume on the neural correlates of attention. This agreement relates both to the implicit framework the authors apply to their studies of attention and also to the brain regions that are implicated. In this epilogue I will attempt to make explicit the framework that is used and will explore the assumptions that underlie the rules used for identifying the sites of attentional modulation and the sources of the modulatory signals. These assumptions have proved very useful, but most still require further investigation. The distinction between bottom-up and top-down processes is a key components of the framework, but is also a potential source of confusion. It seems that bottom-up processing, in the psychological sense of not being under voluntary control, can involve top-down processes in the physiological sense of involving the feedback of neural signals. © 2001 Elsevier Science Ltd. All rights reserved. Keywords: Neural basis of attention; Framework; Brain regions
I was pleased to find that none of the authors in this special issue on attention is asking questions like ‘where is attention in the brain?’ So I need not devote this epilogue to worrying about why some have found it in region X while others have found it in region Y. Instead all are concerned with the mechanisms by which one stimulus rather than another is selected to be at the centre of our attention. All use much the same framework for interpreting their results and these results are remarkably consistent. In the rest of this epilogue I shall try to make explicit the assumptions of the framework used for discussing mechanisms of selective attention. I shall also speculate about the mechanisms of selective attention that the results of these studies suggest.
1. Outline of the framework The framework is largely derived from the biasedcompetition model of Desimone and Duncan [2]. The first assumption is that selection of one stimulus rather * Tel.: +44-207-833-7472. E-mail address: [email protected] (C. Frith).
than another is the result of competition between stimuli (or spatial locations) for which of them will receive further processing. For this competition to occur there must be at least one region in the brain where signals concerning the competing stimuli can interact. The second assumption is that there are two distinct ways in which selection can occur. Bottom-up selection is determined solely by the intrinsic properties of the stimuli; the most salient stimulus wins. Top-down selection is determined by processes that are independent of the stimuli, typically the instruction to attend to one kind of stimulus, which is not necessarily the most salient in bottom-up terms. These top-down processes bias the competition in favour of the pre-specified stimulus. The terms top-down and bottom-up are somewhat ambiguous because they can be used in a physiological sense or a psychological sense. In the physiological sense bottom-up implies purely feedforward influences (say, signals flowing from extra-striate cortex into parietal cortex). In contrast, top-down in the physiological sense implies a reverse influence, involving feedback projections (e.g. signals that flow from parietal cortex to extra-striate cortex). In the psychological sense bottom-up implies that there is no voluntary control over
0028-3932/01/$ - see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S 0 0 2 8 - 3 9 3 2 ( 0 1 ) 0 0 1 2 4 - 5
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C. Frith / Neuropsychologia 39 (2001) 1367–1371
the process of competition, while top-down implies that there is voluntary control. The physiological and psychological senses of these terms may not be equivalent. For instance, psychologically bottom-up effects could in principle involve feedback influences in a physiological sense (see Macaluso and Driver, this volume) The third assumption is that mechanisms for topdown control (in the psychological sense) depend upon the interaction between a site and a source. A site is a region or set of regions in the brain where stimuli are processed and where competition occurs. A source is the region or set of regions in the brain that is the origin of the signal which biases the competition in the site. The long-standing observation on which all the papers in the present volume build is the observation that top-down attention (in the psychological sense, and probably the physiological sense also) modulates activity in sites where the attended stimulus is processed even when the incoming stimulus is held constant.
2. Where does the competition occur? Kaster and Ungerleider (this volume) suggest that competition between visual objects occurs primarily when both objects are within the receptive field of particular neurones. As competing objects are moved further apart then the site of competition is further up cortical visual pathways (i.e. further away from primary visual cortex) since these regions have progressively larger receptive fields. Most imaging studies, however, are designed to put the processing of competing stimuli as far apart in the brain as possible (e.g. separate hemifields, or separate modalities) in order to elicit distinguishable responses from them. In such cases the competition might have to arise in areas receiving signals from both hemi-fields or both modalities. Macaluso and colleagues (see Macaluso and Driver, this volume) have performed a series of experiments addressing this problem. These identify a number of multi-modal areas, which respond to both touch and vision and may do so for both hemi-fields. These include the intra-parietal sulcus (IPS; multimodal, contralateral) and the temporo-parietal junction (TPJ; multimodal, bilateral), both areas that are frequently reported to have a role in selective attention. They also confirm that attention can modulate activity in areas that are not multi-modal, but specific to hemi-field and modality. So how does this modulation occur if the competition initially arises in higher-level regions that do not have this specificity? One obvious possibility is that signals are fed back from such higher-level, multimodal regions to the appropriate uni-modal area. Macaluso and colleagues have provided some more direct evidence for this in a study [11] showing that irrelevant
tactile stimuli occurring in the same spatial location as a visual event can boost activity in contralateral unimodal visual areas, possibly via modulation from IPS. In psychological terms this effect of tactile stimuli on visual activity is bottom-up, since it is stimulus-driven and apparently outside voluntary control, but the effect may be top-down in the physiological sense that signals may be fed back from multimodal regions (possibly IPS) to modulate extra-striate regions of visual cortex. Eimer (this volume) has used ERPs to find the exact timing of related cross-modal attentional effects. He finds that the crossmodal influence can arise in the early, modality-specific components of the ERP ( 100 ms). Is this before there would be time for any effects of feedback to be manifest? One possibility is that the critical competition between stimuli does not occur only following convergence in multimodal areas of association cortex , but earlier in nuclei of the brain stem or midbrain before signals reach primary sensory areas in the cortex. Another possibility is that feedback signals can operate much more quickly than typically thought. For example, there is recent evidence [12] that V5 projections to V1 operate with a very short time course, contradicting the assumption that the influence of feedback projections should always occur late. A third possibility is that the feedback effects can anticipate the target stimulus, being elicited by the cue for the appropriate attentional state.
3. Competition and co-operation A number of the studies in this volume demonstrate that competition is not the only force at work in selective attention. In the cross-modal studies that I have already mentioned, a stimulus in one modality can enhance the response to a stimulus in another modality if both occur in the same spatial location. This is not competition, but co-operation. There is further evidence for such co-operation in several of the studies of Downing et al. (this volume). Attention to movement will enhance activity in the face processing area as well as motion-related areas if it is a face that is moving. Attention to a location can enhance activity in the face processing area if a face appears near the attended location, even if that face itself is not the target of attention. The mechanism for such co-operation may be much like that for competition. Signals from different aspects of the sensory input must presumably be brought together for the interaction to occur. But how does the brain know whether competition or co-operation is appropriate? Downing et al. follow Duncan [6] and others in suggesting that features of the same object will co-operate, while stimuli coming from different objects will compete. This seems to imply that objects must be
C. Frith / Neuropsychologia 39 (2001) 1367–1371
distinguished before competition or co-operation can occur, but common location (and timing) for different features (even in different modalities) may be at least as important as emanation from a common object (see Downing et al., this volume; Macaluso and Driver, this volume). Perhaps the relevant processes can occur at a sub-object level, in a manner analogous to Gestalt grouping principles [3,14]. Stimuli that occur at the same time or in the same place are likely to produce co-operation. An idea along these lines lies behind an interesting suggestion from Marzi et al. (this volume) concerning the basis of extinction in patients with right hemisphere lesions. These patients are typically aware of a single stimulus presented in their left visual field, but are often not aware of this stimulus if something is presented simultaneously in the right visual field. The stimulus in the right visual field is said to extinguish the one on the left. Marzi et al. suggest that, because of the right hemisphere damage, the activity associated with stimuli presented in the left visual field is not only reduced, but also delayed. As a result, in areas where signals from the two hemispheres are combined, signals from the two stimuli may not arrive simultaneously even though they were presented simultaneously. Instead of co-operation, competition ensues which the stronger signal from the right hemi-field will inevitably win. If this account is correct then it should be possible to re-instate co-operation by presenting the object to the left-hemi-field slightly before the one to the right (see Driver and Vuilleumier [5] for evidence that extinction can be reduced when co-operation rather than competition is encouraged by Gestalt grouping).
4. Identifying sources of top-down control Many of the contributors to this special issue are concerned to identify the brain regions that are the source of the signals which enable top-down control of attention. Different criteria are used for this purpose which indicate a number of implicit assumptions about the nature of these control processes.
4.1. Anticipatory acti6ity Because bottom-up processes are entirely driven by the stimulus it is not possible for there to be bottom-up activity that anticipates the stimulus. Therefore any such anticipatory activity may be a marker of top-down control processes. Nobre (this volume) underlines the importance of anticipation in selective attention through her demonstration that attending to a particular point in time can improve stimulus processing in much the same way (and involving much the same brain regions) as attending to a particular place. Hopfinger et al. (this volume) have used an event-related
1369
paradigm to distinguish activity associated with the cue rather than the target in a Posner-like cueing task. They observed activity in parietal and frontal regions in response to the cue, but not to the target. They conclude that these areas are likely to be the source of top-down signals since the activity precedes the appearance of the to-be-attended target. However, they also saw activity in fusiform visual cortex in response to both cue and target. This region of the cortex was almost certainly a site at which target processing takes place. So why is it showing anticipatory activity? This may relate to the ‘base-line shifts’ now observed in a number of studies of attention including those by Kastner and Ungerleider with their colleagues (this volume; see Driver and Frith [4], for a recent review). Their studies show that top-down selective attention (in the psychological sense, and probably the physiological sense also) can cause an increase in base-line activity in posterior sensory areas, detected by analysing epochs in which a stimulus does not actually appear. This activity is certainly a marker of top-down processes, but in this case the region showing the anticipatory activity may be the site rather than the source of the activity.
4.2. Sustained anticipatory acti6ity that does not change with the appearance of the stimulus To distinguish between anticipatory activity in site and source areas, Kastner and Ungerleider (this volume) required that the anticipatory activity also be sustained and have no stimulus-locked component to qualify as a source. Using this criterion they too identify parietal and frontal regions as the source of topdown control. An interesting aspect of this criterion is that it may point up the similarity (if not identity) of selective attention with working memory (in the sense of maintaining information over an interval). Brain regions involved in working memory have likewise been identified on the basis that they show sustained activity over an interval rather than showing activity that is time-locked to the retrieval cue [13]. deFockert et al. [7] have recently demonstrated that performance of a traditional working memory task (remembering a sequence of digits for a few seconds) can interfere with top-down selective attention. Presumably the same brain regions may be the origin of the top-down control signals in both cases.
4.3. The same region is acti6ated no matter what is being attended to It is in the nature of sites that they are specialised for the processing of specific kinds of stimuli. By contrast, a source may be independent of the kind of stimulus that is being attended (although this is just an assumption). Downing et al. (this volume; see also [8]) use the
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C. Frith / Neuropsychologia 39 (2001) 1367–1371
method of conjunction to find regions which were more activated by increasing attentional load across a variety of different tasks. They identified IPS as a key area. I have already mentioned that Macaluso and Driver (this volume) used a conceptually similar approach, identifying regions that were activated independently of modality (vision or touch). They also identified IPS as a key area. However this area was identified by them in a task in which no (psychological) top-down processes were required. As I have already mentioned convergence areas (as in multimodal association cortex) may be needed to permit competition between stimuli even when no top-down control processes are involved. It is important to note than none of the above criteria are purely empirical, as all make assumptions that may turn out to be unwarranted. Even so there is striking agreement between the studies reviewed in this volume and indeed many other studies. Frontal and parietal regions have been consistently activated when attention is achieved through top-down control processes. Rees and Lavie (this volume) go further and suggest that these regions may be associated not just with attention to stimuli, but also with awareness of these stimuli. While activity in stimulus processing sites can occur in the absence of awareness, when the same stimulation produces awareness then additional activity in parietal and frontal areas is typically seen. It is not entirely clear to what extent this is a top-down process in the psychological sense. Consider, for instance, the change blindness experiment recently reported by Beck et al. [1]. On every trial volunteers tried to detect changes, but were only successful on about 50% of those trials on which changes actually occurred. When changes were detected activity was observed in frontal and parietal regions. However, in this case the detection (vs its absence) was not under voluntary control. Was the activity in frontal and parietal regions elicited by the detection or was it the case that, on trials on which frontal and parietal activity happened to be higher prior to the stimulus, changes were more likely to be detected? A similar argument may apply to the various studies of binocular rivalry and ambiguous figures mentioned by Rees and Lavie (this volume). Here also a change of percept (but not of stimulation) was associated with activity in parietal and frontal regions, but this switch of percept does not seem to be under voluntary control. If we are to maintain the idea that these regions are the source of top-down control signals, then it may be that signals involving the same or related areas are required to maintain the percept once it has emerged, and not only to prepare for it in anticipation. The studies by Rees and Lavie (this volume) on the effects of perceptual load on attention provide
evidence that the role of voluntary processes in attention can sometimes be rather small. These studies show that, if the perceptual load of the primary task is low, then the brain activity elicited by irrelevant stimuli increases. This may imply that we do not always have direct voluntary control over processing of irrelevant stimuli. If the capacity is available the irrelevant stimuli may be processed whether we like it or not [9,10]. Indeed, if the primary task is in a different modality (sound) from the irrelevant stimuli (moving dots) then there can even be no effect of load in one modality on processing of distractors in another modality in some situations. However hard the primary task in one modality our brain may still show some response to irrelevant stimuli in another modality. One important aspect of the various tasks used in the load studies is that the irrelevant stimuli were deliberately chosen not to interfere with the primary task, in the sense that they did not have any pre-potent tendencies to elicit competing responses. It is clear from tasks where such interference is possible, such as those reported by Macaluso and Driver in this volume (in which volunteers had to respond to double stimuli in one modality, but not in the other) that attention can modulate responses across competing modalities. Clearly further work is needed on the relation between attention (selecting stimuli) and intention (selecting responses). The concept of top-down processing (in the psychological sense) often appears troublesome because of the implication that there is some highest region (sometimes known as the homunculus) which is the source of ultimate top-down control. Studies of attention are increasingly suggesting that this problem may be more apparent than real. For instance, Lavie’s perceptual load theory ([9,10]; Rees and Lavie, this volume) shows that attentional selectivity can sometimes merely be a secondary consequence of the task being carried out (and the limited capacities it exhausts) rather than the direct result of voluntary control. But surely the selection of the task is still the result of some voluntary control? Can we identify the brain region where the critical homunculus lives? Well, perhaps, but for most of the experimental paradigms studied to date, it may turn out to be in another brain. That is, it may reside in the brain of the experimenter, who was the ultimate source of top-down control in all these studies, having provided clear instructions about what the subject should and should not attend to. Presumably, in daily life, while our attention can likewise sometimes be directed by other people, it can also be directed on the basis of our current motivations. Understanding how motivational processes interact with attentional processes will be a fruitful topic for further imaging studies.
C. Frith / Neuropsychologia 39 (2001) 1367–1371
Acknowledgements The author’s research is supported by the Wellcome Trust. Jon Driver and Richard Frackowiak made some contributions to this epilogue.
References [1] Beck DM, Rees G, Christopher D, Frith CD, Lavie N. Neural correlates of change detection and change blindness. Nature Neuroscience 2001;4(6):645 –650. [2] Desimone R, Duncan J. Neural mechanisms of selective visual attention. Annual Review of Neuroscience 1995;18:193 – 222. [3] Driver J, Baylis GC. Attention and visual object segmentation. In: Parasuraman R, editor. The attentive brain. Cambridge: MIT Press, 1998:299 – 326. [4] Driver J, Frith CD. Shifting baselines in attention research. Nature Reviews Neuroscience 2000;1(2):147 –8. [5] Driver J, Vuilleumier P. Perceptual awareness and its loss in unilateral neglect and extinction. Cognition 2001;79:39 –88.
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[6] Duncan J. Selective attention and the organisation of visual information. Journal of Experimental Psychology, General 1984;113:501 – 17. [7] de Fockert JW, Rees G, Frith CD, Lavie N. The role of working memory in visual selective attention. Science 2001;291:1803 –6. [8] Kanwisher N, Wojciulik E. Visual attention: Insights from brain imaging. Nat Rev Neurosci 2000;1(2):91 – 100. [9] Lavie N. Perceptual load as a necessary condition for selective attention. J Exp Psychol Hum Percept Perform 1995;21(3):452 – 68. [10] Lavie N, Fox E. The role of perceptual load in negative priming. J Exp Psychol Hum Percept Perform 2000;26(3):1038 –52. [11] Macaluso E, Frith CD, Driver J. Modulation of human visual cortex by crossmodal spatial attention. Science 2000;289:1206 –8. [12] Pascual-Leone A, Walsh V. Fast backprojections from the motion to the primary visual area necessary for visual awareness. Science 2001;292:510 – 2. [13] Rowe JB, Toni I, Josephs O, et al. The prefrontal cortex: Response selection or maintenance within working memory? Science 2000;288:1656 – 60. [14] Rubin E. Visuell Wahrgenommene Figuren. Copenhagen: Glydendalske, 1915.
Concluding review
A framework for studying the neural basis of attention Chris Frith * Wellcome Department of Cogniti6e Neurology, Institute of Neurology, Uni6ersity College London, 12 Queen Square, London WC1N 3BG, UK
Abstract There is a high degree of consensus between the contributors to this volume on the neural correlates of attention. This agreement relates both to the implicit framework the authors apply to their studies of attention and also to the brain regions that are implicated. In this epilogue I will attempt to make explicit the framework that is used and will explore the assumptions that underlie the rules used for identifying the sites of attentional modulation and the sources of the modulatory signals. These assumptions have proved very useful, but most still require further investigation. The distinction between bottom-up and top-down processes is a key components of the framework, but is also a potential source of confusion. It seems that bottom-up processing, in the psychological sense of not being under voluntary control, can involve top-down processes in the physiological sense of involving the feedback of neural signals. © 2001 Elsevier Science Ltd. All rights reserved. Keywords: Neural basis of attention; Framework; Brain regions
I was pleased to find that none of the authors in this special issue on attention is asking questions like ‘where is attention in the brain?’ So I need not devote this epilogue to worrying about why some have found it in region X while others have found it in region Y. Instead all are concerned with the mechanisms by which one stimulus rather than another is selected to be at the centre of our attention. All use much the same framework for interpreting their results and these results are remarkably consistent. In the rest of this epilogue I shall try to make explicit the assumptions of the framework used for discussing mechanisms of selective attention. I shall also speculate about the mechanisms of selective attention that the results of these studies suggest.
1. Outline of the framework The framework is largely derived from the biasedcompetition model of Desimone and Duncan [2]. The first assumption is that selection of one stimulus rather * Tel.: +44-207-833-7472. E-mail address: [email protected] (C. Frith).
than another is the result of competition between stimuli (or spatial locations) for which of them will receive further processing. For this competition to occur there must be at least one region in the brain where signals concerning the competing stimuli can interact. The second assumption is that there are two distinct ways in which selection can occur. Bottom-up selection is determined solely by the intrinsic properties of the stimuli; the most salient stimulus wins. Top-down selection is determined by processes that are independent of the stimuli, typically the instruction to attend to one kind of stimulus, which is not necessarily the most salient in bottom-up terms. These top-down processes bias the competition in favour of the pre-specified stimulus. The terms top-down and bottom-up are somewhat ambiguous because they can be used in a physiological sense or a psychological sense. In the physiological sense bottom-up implies purely feedforward influences (say, signals flowing from extra-striate cortex into parietal cortex). In contrast, top-down in the physiological sense implies a reverse influence, involving feedback projections (e.g. signals that flow from parietal cortex to extra-striate cortex). In the psychological sense bottom-up implies that there is no voluntary control over
0028-3932/01/$ - see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S 0 0 2 8 - 3 9 3 2 ( 0 1 ) 0 0 1 2 4 - 5
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C. Frith / Neuropsychologia 39 (2001) 1367–1371
the process of competition, while top-down implies that there is voluntary control. The physiological and psychological senses of these terms may not be equivalent. For instance, psychologically bottom-up effects could in principle involve feedback influences in a physiological sense (see Macaluso and Driver, this volume) The third assumption is that mechanisms for topdown control (in the psychological sense) depend upon the interaction between a site and a source. A site is a region or set of regions in the brain where stimuli are processed and where competition occurs. A source is the region or set of regions in the brain that is the origin of the signal which biases the competition in the site. The long-standing observation on which all the papers in the present volume build is the observation that top-down attention (in the psychological sense, and probably the physiological sense also) modulates activity in sites where the attended stimulus is processed even when the incoming stimulus is held constant.
2. Where does the competition occur? Kaster and Ungerleider (this volume) suggest that competition between visual objects occurs primarily when both objects are within the receptive field of particular neurones. As competing objects are moved further apart then the site of competition is further up cortical visual pathways (i.e. further away from primary visual cortex) since these regions have progressively larger receptive fields. Most imaging studies, however, are designed to put the processing of competing stimuli as far apart in the brain as possible (e.g. separate hemifields, or separate modalities) in order to elicit distinguishable responses from them. In such cases the competition might have to arise in areas receiving signals from both hemi-fields or both modalities. Macaluso and colleagues (see Macaluso and Driver, this volume) have performed a series of experiments addressing this problem. These identify a number of multi-modal areas, which respond to both touch and vision and may do so for both hemi-fields. These include the intra-parietal sulcus (IPS; multimodal, contralateral) and the temporo-parietal junction (TPJ; multimodal, bilateral), both areas that are frequently reported to have a role in selective attention. They also confirm that attention can modulate activity in areas that are not multi-modal, but specific to hemi-field and modality. So how does this modulation occur if the competition initially arises in higher-level regions that do not have this specificity? One obvious possibility is that signals are fed back from such higher-level, multimodal regions to the appropriate uni-modal area. Macaluso and colleagues have provided some more direct evidence for this in a study [11] showing that irrelevant
tactile stimuli occurring in the same spatial location as a visual event can boost activity in contralateral unimodal visual areas, possibly via modulation from IPS. In psychological terms this effect of tactile stimuli on visual activity is bottom-up, since it is stimulus-driven and apparently outside voluntary control, but the effect may be top-down in the physiological sense that signals may be fed back from multimodal regions (possibly IPS) to modulate extra-striate regions of visual cortex. Eimer (this volume) has used ERPs to find the exact timing of related cross-modal attentional effects. He finds that the crossmodal influence can arise in the early, modality-specific components of the ERP ( 100 ms). Is this before there would be time for any effects of feedback to be manifest? One possibility is that the critical competition between stimuli does not occur only following convergence in multimodal areas of association cortex , but earlier in nuclei of the brain stem or midbrain before signals reach primary sensory areas in the cortex. Another possibility is that feedback signals can operate much more quickly than typically thought. For example, there is recent evidence [12] that V5 projections to V1 operate with a very short time course, contradicting the assumption that the influence of feedback projections should always occur late. A third possibility is that the feedback effects can anticipate the target stimulus, being elicited by the cue for the appropriate attentional state.
3. Competition and co-operation A number of the studies in this volume demonstrate that competition is not the only force at work in selective attention. In the cross-modal studies that I have already mentioned, a stimulus in one modality can enhance the response to a stimulus in another modality if both occur in the same spatial location. This is not competition, but co-operation. There is further evidence for such co-operation in several of the studies of Downing et al. (this volume). Attention to movement will enhance activity in the face processing area as well as motion-related areas if it is a face that is moving. Attention to a location can enhance activity in the face processing area if a face appears near the attended location, even if that face itself is not the target of attention. The mechanism for such co-operation may be much like that for competition. Signals from different aspects of the sensory input must presumably be brought together for the interaction to occur. But how does the brain know whether competition or co-operation is appropriate? Downing et al. follow Duncan [6] and others in suggesting that features of the same object will co-operate, while stimuli coming from different objects will compete. This seems to imply that objects must be
C. Frith / Neuropsychologia 39 (2001) 1367–1371
distinguished before competition or co-operation can occur, but common location (and timing) for different features (even in different modalities) may be at least as important as emanation from a common object (see Downing et al., this volume; Macaluso and Driver, this volume). Perhaps the relevant processes can occur at a sub-object level, in a manner analogous to Gestalt grouping principles [3,14]. Stimuli that occur at the same time or in the same place are likely to produce co-operation. An idea along these lines lies behind an interesting suggestion from Marzi et al. (this volume) concerning the basis of extinction in patients with right hemisphere lesions. These patients are typically aware of a single stimulus presented in their left visual field, but are often not aware of this stimulus if something is presented simultaneously in the right visual field. The stimulus in the right visual field is said to extinguish the one on the left. Marzi et al. suggest that, because of the right hemisphere damage, the activity associated with stimuli presented in the left visual field is not only reduced, but also delayed. As a result, in areas where signals from the two hemispheres are combined, signals from the two stimuli may not arrive simultaneously even though they were presented simultaneously. Instead of co-operation, competition ensues which the stronger signal from the right hemi-field will inevitably win. If this account is correct then it should be possible to re-instate co-operation by presenting the object to the left-hemi-field slightly before the one to the right (see Driver and Vuilleumier [5] for evidence that extinction can be reduced when co-operation rather than competition is encouraged by Gestalt grouping).
4. Identifying sources of top-down control Many of the contributors to this special issue are concerned to identify the brain regions that are the source of the signals which enable top-down control of attention. Different criteria are used for this purpose which indicate a number of implicit assumptions about the nature of these control processes.
4.1. Anticipatory acti6ity Because bottom-up processes are entirely driven by the stimulus it is not possible for there to be bottom-up activity that anticipates the stimulus. Therefore any such anticipatory activity may be a marker of top-down control processes. Nobre (this volume) underlines the importance of anticipation in selective attention through her demonstration that attending to a particular point in time can improve stimulus processing in much the same way (and involving much the same brain regions) as attending to a particular place. Hopfinger et al. (this volume) have used an event-related
1369
paradigm to distinguish activity associated with the cue rather than the target in a Posner-like cueing task. They observed activity in parietal and frontal regions in response to the cue, but not to the target. They conclude that these areas are likely to be the source of top-down signals since the activity precedes the appearance of the to-be-attended target. However, they also saw activity in fusiform visual cortex in response to both cue and target. This region of the cortex was almost certainly a site at which target processing takes place. So why is it showing anticipatory activity? This may relate to the ‘base-line shifts’ now observed in a number of studies of attention including those by Kastner and Ungerleider with their colleagues (this volume; see Driver and Frith [4], for a recent review). Their studies show that top-down selective attention (in the psychological sense, and probably the physiological sense also) can cause an increase in base-line activity in posterior sensory areas, detected by analysing epochs in which a stimulus does not actually appear. This activity is certainly a marker of top-down processes, but in this case the region showing the anticipatory activity may be the site rather than the source of the activity.
4.2. Sustained anticipatory acti6ity that does not change with the appearance of the stimulus To distinguish between anticipatory activity in site and source areas, Kastner and Ungerleider (this volume) required that the anticipatory activity also be sustained and have no stimulus-locked component to qualify as a source. Using this criterion they too identify parietal and frontal regions as the source of topdown control. An interesting aspect of this criterion is that it may point up the similarity (if not identity) of selective attention with working memory (in the sense of maintaining information over an interval). Brain regions involved in working memory have likewise been identified on the basis that they show sustained activity over an interval rather than showing activity that is time-locked to the retrieval cue [13]. deFockert et al. [7] have recently demonstrated that performance of a traditional working memory task (remembering a sequence of digits for a few seconds) can interfere with top-down selective attention. Presumably the same brain regions may be the origin of the top-down control signals in both cases.
4.3. The same region is acti6ated no matter what is being attended to It is in the nature of sites that they are specialised for the processing of specific kinds of stimuli. By contrast, a source may be independent of the kind of stimulus that is being attended (although this is just an assumption). Downing et al. (this volume; see also [8]) use the
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method of conjunction to find regions which were more activated by increasing attentional load across a variety of different tasks. They identified IPS as a key area. I have already mentioned that Macaluso and Driver (this volume) used a conceptually similar approach, identifying regions that were activated independently of modality (vision or touch). They also identified IPS as a key area. However this area was identified by them in a task in which no (psychological) top-down processes were required. As I have already mentioned convergence areas (as in multimodal association cortex) may be needed to permit competition between stimuli even when no top-down control processes are involved. It is important to note than none of the above criteria are purely empirical, as all make assumptions that may turn out to be unwarranted. Even so there is striking agreement between the studies reviewed in this volume and indeed many other studies. Frontal and parietal regions have been consistently activated when attention is achieved through top-down control processes. Rees and Lavie (this volume) go further and suggest that these regions may be associated not just with attention to stimuli, but also with awareness of these stimuli. While activity in stimulus processing sites can occur in the absence of awareness, when the same stimulation produces awareness then additional activity in parietal and frontal areas is typically seen. It is not entirely clear to what extent this is a top-down process in the psychological sense. Consider, for instance, the change blindness experiment recently reported by Beck et al. [1]. On every trial volunteers tried to detect changes, but were only successful on about 50% of those trials on which changes actually occurred. When changes were detected activity was observed in frontal and parietal regions. However, in this case the detection (vs its absence) was not under voluntary control. Was the activity in frontal and parietal regions elicited by the detection or was it the case that, on trials on which frontal and parietal activity happened to be higher prior to the stimulus, changes were more likely to be detected? A similar argument may apply to the various studies of binocular rivalry and ambiguous figures mentioned by Rees and Lavie (this volume). Here also a change of percept (but not of stimulation) was associated with activity in parietal and frontal regions, but this switch of percept does not seem to be under voluntary control. If we are to maintain the idea that these regions are the source of top-down control signals, then it may be that signals involving the same or related areas are required to maintain the percept once it has emerged, and not only to prepare for it in anticipation. The studies by Rees and Lavie (this volume) on the effects of perceptual load on attention provide
evidence that the role of voluntary processes in attention can sometimes be rather small. These studies show that, if the perceptual load of the primary task is low, then the brain activity elicited by irrelevant stimuli increases. This may imply that we do not always have direct voluntary control over processing of irrelevant stimuli. If the capacity is available the irrelevant stimuli may be processed whether we like it or not [9,10]. Indeed, if the primary task is in a different modality (sound) from the irrelevant stimuli (moving dots) then there can even be no effect of load in one modality on processing of distractors in another modality in some situations. However hard the primary task in one modality our brain may still show some response to irrelevant stimuli in another modality. One important aspect of the various tasks used in the load studies is that the irrelevant stimuli were deliberately chosen not to interfere with the primary task, in the sense that they did not have any pre-potent tendencies to elicit competing responses. It is clear from tasks where such interference is possible, such as those reported by Macaluso and Driver in this volume (in which volunteers had to respond to double stimuli in one modality, but not in the other) that attention can modulate responses across competing modalities. Clearly further work is needed on the relation between attention (selecting stimuli) and intention (selecting responses). The concept of top-down processing (in the psychological sense) often appears troublesome because of the implication that there is some highest region (sometimes known as the homunculus) which is the source of ultimate top-down control. Studies of attention are increasingly suggesting that this problem may be more apparent than real. For instance, Lavie’s perceptual load theory ([9,10]; Rees and Lavie, this volume) shows that attentional selectivity can sometimes merely be a secondary consequence of the task being carried out (and the limited capacities it exhausts) rather than the direct result of voluntary control. But surely the selection of the task is still the result of some voluntary control? Can we identify the brain region where the critical homunculus lives? Well, perhaps, but for most of the experimental paradigms studied to date, it may turn out to be in another brain. That is, it may reside in the brain of the experimenter, who was the ultimate source of top-down control in all these studies, having provided clear instructions about what the subject should and should not attend to. Presumably, in daily life, while our attention can likewise sometimes be directed by other people, it can also be directed on the basis of our current motivations. Understanding how motivational processes interact with attentional processes will be a fruitful topic for further imaging studies.
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Acknowledgements The author’s research is supported by the Wellcome Trust. Jon Driver and Richard Frackowiak made some contributions to this epilogue.
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