VISUAL ATTENTION 203 204 DESIMONE DUNCAN Top-Down Control of Selection in the Ventral Stream 1ocalizedaregionmodulstedbyspatialatienioninlsiepmlprestnatecortex av-down biases on ss at hand. region may correspond to area V4(Mangun et al 1993). templa e,der e from the requiremen of the Although we Recently,Motter(1993)has reported attentional effects on responses of cells in V1,V2,and V4.In contrast to the Moran Desimone (1985)study,these share many features. effects were found when one stimulus was inside the field,and others outside. Most surprisingly,cueing the animal for the target location was almost as likely to suppress responses to the target as to facilitate them.A possible reason for SELECTION BASED ON SPATIAL LOCATION As we described above,one central the discrepancy between the two studies is that Motter (1993)found these resource for which stimuli compete in the ventral stream seems to be the effects only when there were a large number of distractors in the visual field receptive field.Not surprisingly then,spatial selection in this stream does not whereas Moran&Desimone(1985)used only a single distractor.Increasing simply enhance processing of the stimulus at the attended location but rathe the c competitio objects in the vis have in sed the rol ms to resolve competition between stimuli in the receptive field. Mo study of cells in v4 and It conex monkevs f med a discrim ination task on to stimuli at one ioin the visual d,rn plicit p the target locatio ge (b t not any of the distractors)was physically adde possibly ractors at a seco ran De 85).The on (M he monkey by cing some complex sensory effects.In any event,other recent studies have indi i to confirmed that attenti onal effects in V4 are muc larger when target and t the star of th un,1. the spatial was purer distractor compete within the same receptive field than in any other configu- d spatia mory. ration (Luck et al 1993:L Chelazzi,unpublished data). were both within the receptive field of the recorded cell,the uronal response was determined primarily by the target;responses to the CIRCUTTRY UNDERLYING SPATIAL SELECTION Although the synaptic mecha- distractor The cells responded as though their nisms mediating the gating of V4 and IT responses are unknown,anatomy Ishrunk around the target.Consistent with this,Richmond dictates that they fall into either of two classes (Desimone 1992).In the first et al(1983)found that the presence of a central fixation target in the receptive class,spatial biasing inputs to visual cortex determine which specific subset field of an IT neuron may block the response to a more peripheral stimulus of a cell's inputs causes the cell to fire,whereas in the second class,the inputs in the field. determine which specific cells in a population are allowed to fire.In other In the Moran Desimone (1985)study,when one of the two locations was words.one can either gate some of the inputs to a cell on or off,or one can placed outside the receptive field of the recorded cell.attention no longer had gate some of the cells on or off.Theoretical models for both classes of circuitry any effect on the response.This was consistent with the biased competition have been developed (Anderson Van essen 1987.Crick&Koch 1990 model:Target and distractor were no longer competing for the cell'respor e none 1992 Ni 9g301 eptieheaspatialbiase7 bur et al 1 sen ct al 1993,Tsotsos 1994).All and thus,top-dow had ar effect f the are ouli within th which operated were much larger in the en ent data to he ortex r were loc y. 19 he same hemifield and,there e gating of V an I responses occurs as a res lt of an exteral inpu targ that biases competition in favor of the target,one might expect to see some n competition(Sato 1988). evidence for it.A possible candidate has been found in a new study of spatial receptive field s were too small to test the effects of placing both attention in V4 (Luck et al 1993).V4 cells in this study showed a sustained inoe e a theroVh elevation of their baseline (prestimulus)firing rates whenever the animal's attention was directed inside their receptive field.This elevation of activity was no effect of attention on VI cells in this paradigm.These results suggest with attention could be the neural analogue of the attentional template for that target selection is a two-stage process:The first stage works over a small location.The elevation occurred at the start of each trial before any stimulus spatial range in V4.and the second stage works over a much larger spatial had appeared.Since the only information about where to attend was given to range in IT cortex:both are in line with their receptive field sizes (Moran the animal minutes carlier at the start of a block of trials,the relevant location Desimone 1985).Studies of event-related notentials in hnmans have also met have heen stomed in wnrkino memory The snatial resnlntion nf this sonrre
VISUAL ATq~NTION 203 Top-Down Control of Selection in the Ventral Stream As we have said, top-down biases on visual processing, or the attentional template, derive from the requirements of the task at hand. Although we consider mechanisms for spatial and object selection separately, they in fact share many features. SELECTION BASED ON SPATIAL LOCATION Aswe described above, one central resource for which stimuli compete in the ventral stream seems to be the receptive field. Not surprisingly then, spatial selection in this stream does not simply enhance processing of the stimulus at the attended location but rather seems to resolve competition between stimuli in the receptive field. In one study of cells in V4 and IT cortex, monkeys performed a discrimination task on target stimuli at one location in the visual field, ignoring simultaneously presented distractors at a second location (Moran & Desimone 1985). The target location for a given run was indicated to the monkey by special instruction trials at the start of that run, i.e. the spatial bias was purely top down and presumably required spatial working memory. When target and distractor were both within the receptive field of the recorded cell, the neuronal response was determined primarily by the target; responses to the distractor were greatly attenuated. The cells responded as though their receptive fields had shrunk around the target. Consistent with this, Richmond et al (1983) found that the presence of a central fixation target in the receptive field of an IT neuron may block the response to a more peripheral stimulus in the field. In the Moran & Desimone (1985) study, when one of the two locations was placed outside the receptive field of the recorded cell, attention no longer had any effect on the response. This was consistent with the biased competition model: Target and distractor were no longer competing for the cell’s response, and thus, top-down spatial bias no longer had any effect. Receptive fields and the region of space over which attention operated were much larger in the IT cortex. However, even here attentional effects were larger when target and distractor were located within the same hemifield and, therefore, more likely to be in competition (Sato 1988). In V1, receptive fields were too small to test the effects of placing both target and distractor within them. However, when one stimulus was located inside, and one outside (at the same spatial separation used in area V4), there was no effect of attention on V1 cells in this paradigm. These results suggest that target selection is a two-stage process: The first stage works over a small spatial range in V4, and the second stage works over a much larger spatial range in IT cortex; both are in line with their receptive field sizes (Moran Desimone 1985). Studies of event-related potentials in humans have also www.annualreviews.org/aronline Annual Reviews Annu. Rev. Neurosci. 1995.18:193-222. Downloaded from arjournals.annualreviews.org by University of California - San Diego on 01/05/07. For personal use only. 204 DESIMONE & DUNCAN localized a region modulated by spatial attention in lateral prestriate cortex; this region may correspond to area V4 (Mangun et al 1993). Recently, Motter (1993) has reported attentional effects on responses of cells in V1, V2, and V4. In contrast to the Moran & Desimone (1985) study, these effects were found when one stimulus was inside the field, and others outside. Most surprisingly, cueing the animal for the target location was almost as likely to suppress responses to the target as to facilitate them. A possible reason for the discrepancy between the two studies is that Motter (1993) found these effects only when there were a large number of distractors in the visual field, whereas Moran & Desimone (1985) used only a single distractor. Increasing the competition among objects in the visual field may have increased the role of attentional biases. Other differences include the fact that Motter used an explicit spatial cue to indicate the target location in the display, and the target (but not any of the distractors) was physically added to the cue, possibly inducing some complex sensory effects. In any event, other recent studies have confirmed that attentional effects in V4 are much larger when target and distractor compete within the same receptive field than in any other configuration (Luck et al 1993; L Chelazzi, unpublished data). CIRCUITRY UNDERLYING SPATIAL SELECTION Although the synaptie mechanisms mediating the gating of V4 and IT responses are unknown, anatomy dictates that they fall into either of two classes (Desimone 1992). In the first class, spatial biasing inputs to visual cortex determine which specific subset of a cell’s inputs causes the cell to fire, whereas in the second class, the inputs determine which specific cells in a population are allowed to fire. In other words, one can either gate some of the inputs to a cell on or off, or one can gate some of the cells on or off. Theoretical models for both classes of circuitry have been developed (Anderson & Van Essen 1987, Crick & Koch 1990, Desimone 1992, Niebur et al 1993, Olshausen et al 1993, Tsotsos 1994). All of the models resolve competition when there are mulitple stimuli within the receptive field. Presently, there are insufficient data to decide between them. If the gating of V4 and IT responses occurs as a result of an external input that biases competition in favor of the target, one might expect to see some evidence for it. A possible candidate has been found in a new study of spatial attention in V4 (Luck et al 1993). V4 cells in this study showed a sustained elevation of their baseline (prestimulus) firing rates whenever the animal’s attention was directed inside their receptive field. This elevation of activity with attention could be the neural analogue of the attentional template for location. The elevation occurred at the start of each trial before any stimulus had appeared. Since the only information about where to attend was given to the animal minutes earlier at the start of a block of trials, the relevant location must have been stored in working memory. The spatial resolution of this source www.annualreviews.org/aronline Annual Reviews Annu. Rev. Neurosci. 1995.18:193-222. 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VISUALATTENTION 205 206 DESIMONE DUNCAN receptive field,the magnitude of the e shift varied ccording to the whatever spatial bias signal enters the cortex,it apparently has a spatial reso- lution finer than the receptive field dimensions of v4 celis. SELECTION BASED ON FEATURES The mechanism underlying the selection of 30 objects by their features(when their location is not known in advance)requires a means to hold the sought-after object in working memory and to use this memory (or attentional template)to resolve competition among the elements in the scene.Recently,evidence for this selection mechanism has been found 25 in the anteroventral portion of IT cortex,the same portion in which memory related activity has been found (Chelazzi et al 1993a) briefly pre rotgactoho esented with a co mp ex picture (the cue)at the cent ory.The cue on a goo at elicited a strong espons Good cue icited or no resp onse elf.Fol ⑧15 ga delay,the and the po oth presented nuli,at an extrafoveal lo tion.The monkey made a sacc to the target stimulus that matched the cue,ignoring the nonmatching stimulus (the distractor). As shown in Figure 5.the choice array initially activated IT cells tuned to 小 the properties of either stimulus,in parallel,irrespective of which stimulus was the target.Within 200 ms after array onset,however,the response changed Poor cue dramatically depending on whether the animal was about to make an cye 0 movement to the good or poor stimulus.When the target was the good stimulus .7 00.71.42.12.83.5 the response remained high.However.when the tareet was the poor stimulus for the recorded cell,the resp onse to the good dist actor stimulus was sup Time from cue onset (s) pressed even tho gh ithin ms be ve field.This change Figure 5 Effects ofobject selection onr 100 ocellsinthe ITcore.The upp movemen he general aphs sho erage r the ta ity in IT cortex reflected only th target's prop Whenthe choice animal made a sacc m to the stin and remained ecedighcchaieea suppressed until well after the eye movement was made.Similar effects were the cu ving the delay.celis found for choice arrays of larger sizes. n whe Just as with spatially directed attention,these effects of object selection in s diverged pending o get was the good or th the IT cortex were much smaller when target and nontargets were located in et al (1993ak opposite hemifields than when they were in the same hemifield,i.e.when they were maximally in competition.Interestingly,similar competitive effects are receptive field were more suppressed when the competing target was located seen even at high levels of oculomotor control in the frontal eye field.Cells just ouside the receptive field,and thus maximally competitive,than when it in this region were recorded while monkeys made eye movements to a target was further in a field of distractors(Schall Hanes 1993).Responses to distractors in the Two find sueeest that the taroet is selected in the IT cortex as a result
VISUAL ATTENTION 205 was very high; when attention was shifted to different regions within the same receptive field, the magnitude of the baseline shift varied according to the distance between the focus of attention and the receptive field center. Thus, whatever spatial bias signal enters the cortex, it apparently has a spatial resolution finer than the receptive field dimensions of V4 cells. SELECTION BASED ON FEATURES The mechanism underlying the selection of objects by their features (when their location is not known in advance) requires a means to hold the sought-after object in working memory and to use this memory (or attentional template) to resolve competition among the elements in the scene. Recently, evidence for this selection mechanism has been found in the anteroventral portion of IT cortex, the same portion in which memoryrelated activity has been found (Chelazzi et al 1993a). Monkeys were briefly presented with a complex picture (the cue) at the center of gaze to hold in memory. The cue on a given trial was either a good stimulus that elicited a strong response from the cell or a poor stimulus that elicited little or no response when presented by itself. Following a delay, the good and the poor stimuli were both presented simultaneously as choice stimuli, at an extrafoveal location. The monkey made a saccadic eye movement to the target stimulus that matched the cue, ignoring the nonmatching stimulus (the distractor). As shown in Figure 5, the choice array initially activated IT cells tuned to the properties of either stimulus, in parallel, irrespective of which stimulus was the target. Within 200 ms after array onset, however, the response changed dramatically depending on whether the animal was about to make an eye movement to the good or poor stimulus. When the target was the good stimulus, the response remained high. However, when the target was the poor stimulus for the recorded cell, the response to the good distractor stimulus was suppressed even though it was still within the receptive field. This change in response occurred about 100 ms before the onset of the eye movement. The cells responded as though the target stimulus captured their response, so neuronal activity in IT cortex reflected only the target’s properties. Cells selective for the nontargets were suppressed within 200 ms and remained suppressed until well after the eye movement was made. Similar effects were found for choice arrays of larger sizes. Just as with spatially directed attention, these effects of object selection in the IT cortex were much smaller when target and nontargets were located in opposite hemifields than when they were in the same hemifield, i.e. when they were maximally in competition. Interestingly, similar competitive effects are seen even at high levels of oculomotor control in the frontal eye field. Cells in this region were recorded while monkeys made eye movements to a target in a field of distractors (Schall & Hanes 1993). Responses to distractors in the www.annualreviews.org/aronline Annual Reviews Annu. Rev. Neurosci. 1995.18:193-222. Downloaded from arjournals.annualreviews.org by University of California - San Diego on 01/05/07. For personal use only. 206 DESIMONE & DUNCAN 30- 25- 20- ~15- ,., ~ -- Poor cue ,,-~, -0.7 0 0.7 1.4 2.1 2.8 3.5 Time from cue onset (s) Figure5 Effects ofobject selection on responses of cells in the IT cortex. The upper insert illustrates the general visual search task. Graphshow the average response of 22 cells recorded while monkeys performed the task. The cue was chosen to be either a good or a poor stimulus for the recorded cell. When the choice array was presented, the animal made a saccadic eye movement to the stimulus (target) that matched the previous cue. The saccadic latency was 300 ms, indicated by the asterisk. Cells had a higher firing rate in the delay preceding the choice array when their prefered stimulus was the cue. Following the delay, cells were activated (on the average) by their prefered stimulus the array, regardless of whether it was the target. However, 100 ms before the eye movement was made, responses diverged depending on whether the target was the good or the poor stimulus. The two dark horizontal bars indicate when the cue and the choice were presented. Adapted from Chelazzi et al (1993a). receptive field were more suppressed when the competing target was located just outside the receptive field, and thus maximally competitive, than when it was further away. Two findings suggest that the target is selected in the IT cortex as a result www.annualreviews.org/aronline Annual Reviews Annu. Rev. Neurosci. 1995.18:193-222. Downloaded from arjournals.annualreviews.org by University of California - San Diego on 01/05/07. For personal use only