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 ration (Luck et al 1993:L Chelazzi,unpublished data).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 sonrreVISUAL 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 discrim￾ination 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, there￾fore, 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 configu￾ration (Luck et al 1993; L Chelazzi, unpublished data). CIRCUITRY UNDERLYING SPATIAL SELECTION Although the synaptie mecha￾nisms 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. Downloaded from arjournals.annualreviews.org by University of California - San Diego on 01/05/07. For personal use only