VISUAL ATTENTION 211 212 DESIMONE DUNCAN one quadrant of the In on study,anim we make eye movements to an od -ma nimpp 1976. around an imaginary ring(Schiller&Lee 1991).If the target was located in eye movements rather than in selection for visual processing.A remarkable the lesion quadrant and if it was dimmer than the other stimuli in the unaffected implication of the fact that these visuomotor cells respond equally to targets parts of the field,the animals were impaired.However,there was no impair and distractors in the absence of eye movements is that visual input to these ment if the target was brighter than the other stimuli,suggesting that the V4 parts of the oculomotor system does not derive from cells in the dorsal and lesion reduced target saliency.In another study,animals were especially im- ventral streams whose responses are gated by spatial attention.Competition paired in discriminating the shape of a target located in the lesion quadrant between stimuli must take place inder ndently within the oculomotor system when a distractor was located in an unaffcc d part of the field:however.there and yet be coordinated with competition within visual pr cessing systems was little impai rment when both the target and distractor were located within Although cells in the substantia nigra and intermediate layer of the col- the lesion adrant (Desimone et al 1990a).In the latter configurat ion,neither licnlus have not yet been tested in this condition of attentio n withou mulus had a co etitive advantage from the lesic lsin Pdm,dorsolateral p cummary,the 0 atit odel affo explanation for 1981.c cem this pure the effects I this tir the pulvin B 19 93b o more likely tha t es to be a cri etal 1985).Of the the po enor pane o the ven tral stream.To pin down th sources wil kely require converging may be th on,as th evidence from lesion and physiological studies simply reflect the ves from s with PET have shown activation parietal c Po parietal cortex PHYSIOLOGICAL STUDIES The classic paradigm for studying cells within the a task involving shifting attention (Corbetta et al 1993).Thus,based on pres presumed control system for spatial attention has been the saccadic enhance ence of the cnhancement citect.both postenor panctal and pretrontal cortex ment paradigm (Goldberg Wurtz 1972.Wurtz Goldberg 1972).In this are possible sources of a spatial-biasing signal to visual cortex. task.the monkey fixates a central stimulus while a second stimulus is presented If the top-down selection of spatial locations for attention typically involves within a cell's receptive field in the periphery.in the experimental condition working memory.as we have suggested,an important clue to the identity of the fixation stimulus is turned off and the nal saccades to the re the relevant cells would be respo nse activation in workine memory tasks in field stimulus when it a rs.In a cont rol condition.the fixation fact.in such tasks cells in the dorsolateral prefrontal and oosterior parictal tays on and the arded fo are tonically active whenever the animal holds"in mind"a location c field stim ng when itdims,ign us The ntrol onng the ehtheexperimentalcoiditionHaso m s is la op dow within a cell's receptive field (in the absence of any stimulus)(Chelazzi et al omatic,or re al 1993 di pelli o Wise 1993a.Funahashi e时a11989 Fuster 1973,Gn 988,0u a&Fuster 1992,Wilson et al o the receptive field stimus in the expermentalo 993).Furth ore,these t om appear to. ted system tion (the target) than in the control (the distractor),a resui usually terme see Goldman-Rakic 1988).These physiol Idata,in conju the enhancement effect(although,in fact,it is often unclear whether the targe with data showing neglect and extinction effects following both prefronta response is enhanced or the distractor response is suppressed).This effect is posterior parietal lesions,argue that both structures may work together in found in the superior colliculus.the substantia nigra.the Pdm nucleus of the generating top-down spatial selection biases. pulvinar,the posterior parietal cortex.the frontal eye fields(Goldberg&Wurtz 1972.Hikosaka wurtz 1983.Lynch et al 1977 Robinson et al 1978.Petersen Sources of Object Selection Bias et al 1985,Wurtz Mohler 1976;also see Colby 1991),and the dorsolateral As with spatial selection,the attentional templates for objects and their features prefrontal cortex (di Pelligrino Wise 1993b).However,in both the superfi- may derive from mechanisms underlying working memory.If so,then the cial layers of the colliculus and the frontal eye fields,the effect is known to prefrontal cortex most likely plays an important role.Just as lesions of the be specific for saccadic eye movements:no enhancement is found when the dorsolateral prefrontal cortex impair working memory for space(see FunahashiVISUAL ATTENTION 211 an outcome is observed in monkeys with lesions affecting one quadrant of the visual field representation in area V4. In one study, animals were trained to make eye movements to an odd-man-out target in an array of stimuli presented around an imaginary ring (Schiller & Lee 1991). If the target was located the lesion quadrant and if it was dimmer than the other stimuli in the unaffected parts of the field, the animals were impaired. However, there was no impair￾ment if the target was brighter than the other stimuli, suggesting that the V4 lesion reduced target saliency. In another study, animals were especially im￾paired in discriminating the shape of a target located in the lesion quadrant when a distractor was located in an unaffected part of the field; however, there was little impairment when both the target and distractor were located within the lesion quadrant (Desimonet al 1990a). In the latter configuration, neither stimulus had a competitive advantage from the lesion. In summary, the biased competition model affords a ready explanation for the effects of unilateral or partial lesions on attention. At this time, the pulvinar is no more likely than other structures to be a critical source of gating inputs to the ventral stream. To pin down these sources will likely require converging evidence from lesion and physiological studies. PHYSIOLOGICAL STUDIES The classic paradigm for studying cells within the presumed control system for spatial attention has been the saccadic enhance￾ment paradigm (Goldberg & Wurtz 1972, Wurtz & Goldberg 1972). In this task, the monkey fixates a central stimulus while a second stimulus is presented within a cell’s receptive field in the periphery. In the experimental condition, the fixation stimulus is turned off and the animal saccades to the receptive field stimulus when it appears. In a control condition, the fixation stimulus stays on and the monkey is rewarded for signaling when it dims, ignoring the receptive field stimulus. The control over eye movements is largely top down in this task, although the experimental condition has some automatic, or re￾flexive, components. Some of the cells in virtually all structures implicated in spatial attention give larger responses to the receptive field stimulus in the experimental con￾dition (the target) than in the control (the distractor), a result usually termed the enhancement effect (although, in fact, it is often unclear whether the target response is enhanced or the distractor response is suppressed). This effect is found in the superior colliculus, the substantia nigra, the Pdm nucleus of the pulvinar, the posterior parietal cortex, the frontal eye fields (Goldberg & Wurtz 1972, Hikosaka & Wurtz 1983, Lynch et al 1977, Robinson et al 1978, Petersen et al 1985, Wurtz & Mohler 1976; also see Colby 1991), and the dorsolateral prefrontal cortex (di Pelligrino & Wise 1993b). However, in both the superfi￾cial layers of the colliculus and the frontal eye fields, the effect is known to be specific for saccadic eye movements; no enhancement is found when 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. 212 DESIMONE & DUNCAN animal simply attends to the peripheral stimulus and signals when it dims by releasing a bar (Colby et al 1993, Goldberg & Bushnell 1981, Wurtz & Mohler 1976). Thus, these cells appear to be involved in the selection of targets for eye movements rather than in selection for visual processing. A remarkable implication of the fact that these visuomotor cells respond equally to targets and distractors in the absence of eye movements ithat visual input to these parts of the oculomotor system does not derive from cells in the dorsal and ventral streams whose responses are gated by spatial attention. Competition between stimuli must take place independently within the oculomotor system and yet be coordinated with competition within visual processing systems. Although cells in the substantia nigra and intermediate layers of the col￾liculus have not yet been tested in this condition of attention without eye movements, cells in Pdm, dorsolateral prefrontal cortex, and posterior parietal cortex all show the enhancement effect in this purely attentional condition (Bushnell et al 1981, Colby et al 1993, di Pelligrino & Wise 1993b, Petersen et al 1985). Of these three regions, the posterior parietal and prefrontal cortices may be the most critical for spatial attention, as the enhancement in Pdm may simply reflect the input it receives from the posterior parietal cortex. Further￾more, studies with PET have shown activation of posterior parietal cortex in a task involving shifting attention (Corbetta et al 1993). Thus, based on pres￾ence of the enhancement effect, both posterior parietal and prefrontal cortex are possible sources of a spatial-biasing signal to visual cortex. If the top-down selection of spatial locations for attention typically involves working memory, as we have suggested, an important clue to the identity of the relevant cells would be response activation in working memory tasks. In fact, in such tasks cells in the dorsolateral prefrontal and posterior parietal cortexes are tonically active whenever the animal holds "in mind" a location within a cell’s receptive field (in the absence of any stimulus) (Chelazzi et 1993b, Colby et al 1993, di Pelligrino & Wise 1993a, Funahashi et al 1989, Fuster 1973, Gnadt & Andersen 1988, Quintana & Fuster 1992, Wilson et al 1993). Furthermore, these two regions are heavily interconnected anatomically and appear to form part of a distributed system for spatial cognition (for review, see Goldman-Rakic 1988). These physiological data, in conjunction with data showing neglect and extinction effects following both prefrontal and posterior parietal lesions, argue that both structures may work together in generating top-down spatial selection biases. Sources of Object Selection Bias As with spatial selection, the attentional templates for objects and their features may derive from mechanisms underlying working memory. If so, then the prefrontal cortex most likely plays an important role. Just as lesions of the dorsolateral prefrontal cortex impair working memory for space (see Funahashi 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