The role of neural mechanisms of attention in solving the binding problem.

Abstract

For purposes of this review, we will define the binding problem as the problem of how the visual system correctly links up all the different features of complex objects. For example, when viewing a person seated in a blue car, one effortlessly sees that the person's nose belongs to his face and not to the car, and that the car, but not the nose, is blue. To fully understand the solution to this problem requires a good neurobiological theory of object recognition, which does not exist. We will therefore follow the lead of the computer engineer, who, when asked to describe how he would write a computer program to recognize a chicken, replied, “first, assume a spherical chicken.” Thus, in this review we will make some assumptions that simplify the binding problem in order to appreciate how neural mechanisms of attention provide a partial solution. Before getting to the mechanisms of attention, it is useful to consider the psychological and physiological evidence that the binding problem even exists. The classic psychological evidence comes from studies of “illusory conjunctions” (623Treisman A. Schmidt H. Illusory conjunctions in the perception of objects.Cogn. Psychol. 1982; 14: 107-141Crossref PubMed Scopus (0) Google Scholar, 101Cohen A. Ivry R.B. Illusory conjunctions inside and outside the focus of attention.J. Exp. Psychol. Hum. Percept. Perform. 1989; 15: 650-663Crossref PubMed Scopus (94) Google Scholar, 260Ivry R.B. Prinzmetal W. Effect of feature similarity on illusory conjunctions.Percept. Psychophys. 1991; 49: 105-116Crossref PubMed Google Scholar, 20Arguin M. Cavanagh P. Joanette Y. Visual feature integration with an attention deficit.Brain Cogn. 1994; 24: 44-56Crossref PubMed Scopus (24) Google Scholar, 470Prinzmetal W. Henderson D. Ivry R. Loosening the constraints on illusory conjunctions assessing the roles of exposure duration and attention.J. Exp. Psychol. Hum. Percept. Perform. 1995; 21: 1362-1375Crossref PubMed Google Scholar). In a typical experiment, human subjects are briefly presented with an array containing several different objects, such as letters of the alphabet, shown in different colors. In one condition, subjects are cued to attend to one of the letters, and in a comparison condition their attention is divided between the array and another object. In the former condition, with undivided attention, the letter is perceived correctly. However, in the latter condition, with divided attention, subjects often perceive the wrong combinations of letters and colors, e.g., a red letter B and green letter C are misperceived as a green B and a red C. That is, color and shape are incorrectly bound. These studies argue that the binding problem exists and that attention helps to solve it. Consistent with this interpretation, damage to the parietal lobes, which are thought to be involved in allocating attention, can result in illusory conjunctions during free viewing. Patient R. M. suffered two successive strokes that caused extensive bilateral parietooccipital lesions that spared the temporal and frontal lobes. He was severely impaired in attentionally demanding visual tasks, and, when presented with two colored letters, he often misconjoined their identities and colors, even after viewing for up to 10 s (179Friedman-Hill S.R. Robertson L.C. Treisman A. Parietal contributions to visual feature binding evidence from a patient with bilateral lesions.Science. 1995; 269: 853-855Crossref PubMed Google Scholar). By contrast, he was much less impaired on less attentionally demanding tasks such as detecting a “popout” stimulus. The physiological evidence for the binding problem comes from studies of neurons in extrastriate visual cortex of primates. 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However, as one moves through the ventral visual stream that underlies object recognition (636Ungerleider L.G. Mishkin M. Two cortical visual systems.in: Ingle D.J. Goodale M.A. Mansfield R.J.W. Analysis of Visual Behavior. MIT Press, Cambridge, MA1982Google Scholar), the receptive field size of neurons increases steadily. Neurons in area V4, for example, typically have receptive fields that are several degrees wide near the representation of the center of gaze, and neurons in the inferior temporal (IT) cortex have receptive fields that can include the entire central visual field, on both sides of the vertical midline (130Desimone R. Albright T.D. Gross C.G. Bruce C. Stimulus-selective properties of inferior temporal neurons in the macaque.J. Neurosci. 1984; 4: 2051-2062PubMed Google Scholar, 128Desimone R. Schein S. Visual properties of neurons in area V4 of the macaque sensitivity to stimulus form.J. Neurophysiol. 1987; 57: 835-868PubMed Google Scholar, 187Gattass R. Sousa A.P. 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As receptive fields become larger and larger at each processing stage of the ventral stream, there is therefore an increasing number of erroneous feature bindings to rule out. Thus, the binding problem emerges as a necessary consequence of the large receptive fields found in higher-order areas. A possible solution to the binding problem was suggested by the study of 398Moran J. Desimone R. Selective attention gates visual processing in the extrastriate cortex.Science. 1985; 229: 782-784Crossref PubMed Google Scholar, who found that when two stimuli appear within the receptive field of a neuron in either area V4 or inferior temporal cortex, the response elicited by the pair depends on which of the two stimuli is attended. They chose the shape and color of the stimuli such that one of the stimuli elicited a strong response when it was presented alone (the preferred stimulus), whereas the other elicited a very weak response when it was presented alone (the poor stimulus). When attention was directed to the preferred stimulus, the pair elicited a strong response. However, when attention was directed to the poor stimulus, the identical pair elicited a weak response, even though the preferred stimulus was still in its original location (see Figure 1). 353Luck S.J. Chelazzi L. Hillyard S.A. Desimone R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex.J. Neurophysiol. 1997; 77 (a): 24-42PubMed Google Scholar and 487Reynolds J. Chelazzi L. Desimone R. Competitive mechanisms subserve attention in macaque areas V2 and V4.J. Neurosci. 1999; 19: 1736-1753PubMed Google Scholar replicated this result in area V4 and found it to hold in area V2 as well. 626Treue S. Maunsell J.H.R. Attentional modulation of visual motion processing in cortical areas MT and MST.Nature. 1996; 382: 539-541Crossref PubMed Scopus (552) Google Scholar have reported the same pattern of results in areas MT and MST. They presented a preferred stimulus (a dot moving in the cell's preferred direction) together with a poor stimulus (a dot simultaneously moving in the opposite direction) within the receptive field. The responses elicited by the pair were higher when attention was directed to the dot moving in the preferred direction, relative to when attention was directed to the dot moving in the opposite direction. A similar experiment recently conducted by 534Seidemann E. Newsome W.T. Effect of spatial attention on the responses of area MT neurons.J. Neurophysiol. 1999; 81: 1783-1794PubMed Google Scholar also found that when two stimuli appear within the receptive field of an MT neuron, attention to the more-preferred stimulus increases responses, relative to when attention is directed to the poorer stimulus. However, the magnitude of these effects was much smaller than that observed by 626Treue S. Maunsell J.H.R. Attentional modulation of visual motion processing in cortical areas MT and MST.Nature. 1996; 382: 539-541Crossref PubMed Scopus (552) Google Scholar, suggesting that the degree to which attention is able to modulate neuronal responses and the stage of processing at which this occurs may be task dependent. One way to account for these results is to assume that when attention is directed to one of two stimuli within a cell's receptive field, this causes the receptive field to constrict around the attended stimulus, leaving the unattended stimulus outside the receptive field (see Figure 2). According to this interpretation, when attention is directed to the preferred stimulus, the neuron is driven by the preferred stimulus, and its response is therefore large. When attention is directed to the poor stimulus, the preferred stimulus is now excluded from the receptive field, the cell is driven by the poor stimulus, and its response is small. Thus, according to this interpretation, attention solves the binding problem by increasing the effective spatial resolution of the visual system so that even neurons with multiple stimuli inside their large receptive fields process information only about stimuli at the attended location. Further support for the idea that attention increases the spatial resolution of the visual system comes from two recent psychophysical studies. In one (698Yeshurun Y. Carrasco M. Spatial attention improves performance in spatial resolution tasks.Vision Res. 1999; 39: 293-306Crossref PubMed Scopus (160) Google Scholar), subjects were tested in three different tasks that required them to make fine spatial discriminations. In all three tasks, subjects responded more slowly and less accurately when the stimulus appeared at more peripheral locations, where receptive fields are larger. And, in all three tasks, directing attention to the location of the stimulus resulted in faster and more accurate performance. In a related study, 697Yeshurun Y. Carrasco M. Attention improves or impairs visual performance by enhancing spatial resolution.Nature. 1998; 396: 72-75Crossref PubMed Scopus (284) Google Scholar also found that attention paradoxically impairs performance in a task that requires processing of low–spatial frequency components of a stimulus. Subjects were asked to detect the presence of a texture-defined target, which required integration of information at low spatial resolution. Unlike most visual tasks, performance on this detection task is poorer at the fovea than it is at mid-peripheral locations, where spatial resolution is most appropriate for the task (133DeValois R.L. DeValois K.K Spatial Vision. Oxford University Press, New York1988Google Scholar, 215Graham N Visual Pattern Analyzers. Oxford University Press, New York1989Crossref Google Scholar). Yeshurun and Carrasco found that attention improved performance on this task at peripheral locations, presumably by increasing the spatial resolution of peripheral vision to better fit the task. Strikingly, attention significantly reduced performance on the foveal task, where further improvement of spatial resolution would be expected to undermine performance. 127Desimone R. Duncan J. Neural mechanisms of selective visual attention.Annu. Rev. Neurosci. 1995; 18: 193-222Crossref PubMed Google Scholar have proposed that such changes in spatial resolution may emerge as a result of competitive interactions between stimuli. According to this hypothesis, multiple stimuli in the visual field activate populations of neurons that engage in competitive interactions, possibly mediated through local, intracortical connections. When subjects are instructed to attend (or choose voluntarily to attend) to a stimulus at a particular location or with a particular feature, this generates signals within areas outside visual cortex. These signals are then fed back to extrastriate areas, where they bias the competition in these areas in favor of neurons that respond to the features or location of the attended stimulus. As a result, neurons that respond to the attended stimulus remain active while suppressing neurons that respond to the ignored stimuli. In other words, neuronal responses are now determined by the attended stimulus, and any unattended stimuli are filtered out of their classical receptive fields—an effective increase in the neurons' spatial selectivity. For example, imagine recording from a neuron that responds vigorously to stimulus A and fails to respond to stimulus B. If attention is directed to stimulus A, this will bias the competition in favor of the population of cells that normally responds to A, and the cell being recorded will remain active. If attention is then directed to stimulus B, the competing population will win, and the cell being recorded will be suppressed, along with the other members of its population. In retinotopically organized areas, such as area V4, this competition is thought to be strongest for cells located near to one another in the cortex, which therefore share similar receptive fields. We recently tested this idea that attention works through competitive processes by recording V2 and V4 neuronal responses in a behavioral paradigm that allowed us to isolate automatic sensory processing mechanisms from attentional ones (487Reynolds J. Chelazzi L. Desimone R. Competitive mechanisms subserve attention in macaque areas V2 and V4.J. Neurosci. 1999; 19: 1736-1753PubMed Google Scholar). We first tested cells for competitive interactions in the absence of attention. While the monkey attended to a location far outside the receptive field of the neuron, we measured the response to a single reference stimulus within the receptive field. We then compared this response to the response when a probe stimulus was added within the receptive field. When the probe was added to the field, the neuron's response was drawn toward the response that would have been elicited if the probe had appeared alone. For example, the response to a preferred reference stimulus was typically suppressed when a poor stimulus was added as a probe, even when the poor stimulus elicited small excitatory responses when it appeared alone. Symmetrically, the response of the cell increased when a preferred probe stimulus was added to a poor reference stimulus. Thus, the response of a cell to two stimuli in its field is not the sum of its responses to both but rather is a weighted average of its response to each alone. To test how attention influenced this automatic competitive mechanism, we then had the monkey attend to the reference stimulus. The effect of attending to the reference stimulus was to almost precisely eliminate the excitatory or suppressive effect of the probe. If, in the absence of attention, the probe stimulus had suppressed the response to the reference, then attending to the reference restored the cell's response to the level that had been elicited when the reference was presented alone (Figure 3A). Conversely, if the probe stimulus had increased the cell's response, attending to the reference stimulus drove the response down to the level that had been recorded when the reference was presented alone (Figure 3B). Thus, the effect of attention was to modulate the underlying competitive interaction between stimuli. Given the close similarities between attention effects in the dorsal and ventral streams, it seems likely that both streams use the same underlying competitive circuit. Consistent with this possibility, studies of neuronal responses to multiple stimuli have found opponent direction suppression in areas MT and MST of the dorsal stream (474Qian N. Andersen R.A. Transparent motion perception as detection of unbalanced motion signals. II. Physiology.J. Neurosci. 1994; 14: 7367-7380PubMed Google Scholar, 480Recanzone G.H. Wurtz R.H. Schwarz U. Responses of MT and MST neurons to one and two moving objects in the receptive field.J. Neurophysiol. 1997; 78: 2904-2915PubMed Google Scholar; see also 389Mikami A. Newsome W.T. Wurtz R.H. Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT.J. Neurophysiol. 1986; 55: 1308-1327PubMed Google Scholar). Responses to stimuli moving in a nonpreferred direction are increased by the addition of a second stimulus moving in the preferred direction in the receptive field, and, conversely, responses to preferred stimuli are suppressed by the addition of a stimulus moving in the null direction. It remains for future studies to confirm that attention modulates this underlying competitive circuit. Recent functional magnetic resonance imaging (fMRI) experiments in humans support the idea of attentional modulation of an underlying sensory competition. 272Kastner S. De Weerd P. Desimone R. Ungerleider L.G. Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI.Science. 1998; 282: 108-111Crossref PubMed Scopus (518) Google Scholar compared the average fMRI signal elicited by a stimulus when it was presented alone versus the signal elicited when the same stimulus appeared simultaneously with other stimuli (Figure 4A). They found that when attention was directed away to another location, the presence of the additional stimuli reduced the strength of the fMRI signal in the human analogs of monkey V4 and TEO, areas whose receptive fields are large enough to encompass multiple stimuli (Figure 4B). This suppressive effect was minimized when stimuli were separated from one another in space, consistent with the idea that competition is greatest for stimuli occupying the same receptive field. Suppression was weakest in primary visual cortex, whose smaller receptive fields would rarely be expected to process information from more than one of the stimuli, resulting in minimal interactions between stimuli. When subjects were instructed to attend to stimuli at one of the locations, this eliminated most of the suppressive effect of the distractor stimuli, consistent with the physiological results in monkeys. These experiments provide support for the idea that illusory conjunctions are resolved when attentional feedback signals bias an underlying competitive circuit, causing neurons to respond exclusively to the attended stimulus. Possibly the most direct physiological evidence for this predicted bias was reported by 353Luck S.J. Chelazzi L. Hillyard S.A. Desimone R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex.J. Neurophysiol. 1997; 77 (a): 24-42PubMed Google Scholar, who found that attending to a position within the receptive field of a neuron increased its spontaneous firing rate. The spontaneous activity of V2 and V4 neurons increased by 30%–40% when attention was directed to the location of the receptive field, even when the field contained no stimulus. A recent fMRI study in humans has found similar evidence for a sustained increase in activity with attention in the absence of visual stimulation, with the increases occurring at the retinotopic locus of the attended location in the visual field (273Kastner S. Pinsk M.A. De Weerd P. Desimone R. Ungerleider L.G. Increased activity in human visual cortex during directed attention in the absence of visual stimulation.Neuron. 1999; 22: 751-761Abstract Full Text Full Text PDF PubMed Scopus (784) Google Scholar). This effect was found in several cortical visual areas of the dorsal and ventral streams. In the physiological study of 353Luck S.J. Chelazzi L. Hillyard S.A. Desimone R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex.J. Neurophysiol. 1997; 77 (a): 24-42PubMed Google Scholar, the shift in firing rate was largest when the monkey attended to the “hot spot” of the receptive field, where stimuli elicited the strongest response, and was smallest when attention was directed toward the edge of the field. Thus, consistent with its putative role in selecting out one of several stimuli from within the receptive field, the attentional signal that gives rise to this change in spontaneous firing rate has a higher spatial resolution than the receptive field. The bias in favor of an attended stimulus or location is also evidenced by an increase in response to a stimulus at an attended location, which has been found in many, but not all, physiological studies. With just a single stimulus inside the receptive field, 561Spitzer H. Desimone R. Moran J. 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