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EDITORIAL FOCUS
Researchers have long speculated that the spatial-attention and eye-movement systems may share common neural substrates, a view that has received some physiological support recently (e.g., Corbetta et al. 1998
; Ignashchenkova et al. 2004; Kustov and Robinson 1996; Moore and Fallah 2001). In the present article, Fecteau et al. investigate the neural correlates of attention in the SC of monkeys performing a variant of Posner's (1980) cueing paradigm. In this classic paradigm, the reaction time required to make a saccadic or manual response to a target is used as a measure of attention at the target location. When a cue is flashed at the future location of the target, attention is automatically drawn, resulting in shorter reaction times to the subsequent target at that location. The initial capture of attention is followed a short time later by a decline in attention, known as the inhibition of return (IOR) (Posner and Cohen 1984), at the cued location. During the past 20 years, these observations have inspired a large body of research examining the time course and conditions under which attentional capture and IOR operate. In recent work, the authors established the presence of a neural correlate of attentional capture and IOR in the visual responses of SC neurons. During attentional capture, target-related activity at the cued location is increased and saccades to the target are triggered earlier (Bell et al. 2004). During IOR, this visual activity is reduced and saccades are delayed (Bell et al. 2004; Dorris et al. 2002). By varying the time between cue and target, the authors map out a detailed picture of the correlation between SC visual activity and the time course of attention as measured by saccade latency. The results would have gratified James, who speculated that "attention . . . will prepare the motor centers, and shorten the work which a stimulus has to perform on them, to produce a given effect when it comes."
The present article examines the extent to which these behavioral and SC correlates of attentional capture and IOR are modulated by goal-driven (volitional) factors. Fecteau et al. address this question within the cueing paradigm by manipulating the informativeness of the cue. They find that the initial visual response to the cue does not depend on its informativeness but that cue informativeness significantly modulates the later cue- and target-related responses. These changes in SC activity correspond closely with changes in saccade latency, confirming that the monkeys are correctly interpreting the informativeness of the cue. The results clearly show that SC visual responses are influenced by both goal-driven and automatic attentional mechanisms. Interestingly, Fecteau et al.'s behavioral and neural measures suggest that goal-driven mechanisms cannot completely override the automatic time course of attention. Such a result was anticipated by early empiricists, as Helmholtz (1867) suggested, "The relation of attention to will . . . is less one of immediate than of mediate control."
These results lead naturally to the question of whether the SC is involved in generating attentional capture and IOR or whether its role is more limited. Some studies have suggested SC involvement in the automatic capture of attention (Ignashchenkova et al. 2004; Kustov and Robinson 1996), and lesion studies in humans have indicated that the SC may also play a role in generating IOR (Posner et al. 1985; Sapir et al. 1999). On the other hand, a study in monkeys suggests that upstream structures are the source of the IOR-related reduction in SC visual activity (Dorris et al. 2002). Under this latter view, SC activity related to IOR can be regarded as a virtual readout of neural activity present across a network of areas involved in coding stimulus salience. Clearly, there is still much to learn, but renewed interest and research along these lines promises finally to answer many of the questions about attention that captivated James and his contemporaries more than a century ago.
The Smith-Kettlewell Eye Research Institute, San Francisco, California 94115
Address for reprint requests and other correspondence: R. M. McPeek, The Smith-Kettlewell Eye Research Institute, 2318 Fillmore St., San Francisco, CA 94115 (E-mail: rmm{at}ski.org).
REFERENCES
Bell AH, Fecteau JH, and Munoz DP. Using auditory and visual stimuli to investigate the behavioral and neuronal consequences of reflexive covert orienting. J Neurophysiol 91: 2172–2184, 2004.
Corbetta M, Akbudak E, Conturo TE, Snyder AZ, Ollinger JM, Drury HA, Linenweber MR, Petersen SE, Raichle ME, Van Essen DC, and Shulman GL. A common network of functional areas for attention and eye movements. Neuron 21: 761–773, 1998.[CrossRef][ISI][Medline]
Dorris MC, Klein RM, Everling S, and Munoz DP. Contribution of the primate superior colliculus to inhibition of return. J Cog Neurosci 14: 1256–1263.
Fecteau JH, Bell AH, and Munoz DP. Neural correlates of the automatic and goal-driven biases in orienting spatial attention. J Neurophysiol 92: 1728–1737, 2004.
Helmholtz H. Handbuch der Physiologisehen Optik (Dritte Auflage). Hamburg: Voss, 1867. Translation in: James W. The Principles of Psychology. Cambridge, MA: Harvard Univ. Press, 1890.
Ignashchenkova A, Dicke PW, Haarmeier T, and Thier P. Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention. Nat Neurosci 7: 56–64, 2004.[CrossRef][ISI][Medline]
James W. The Principles of Psychology. Cambridge, MA: Harvard Univ. Press, 1890.
Kustov AA and Robinson DL. Shared neural control of attentional shifts and eye movements. Nature 384: 74–77, 1996.[CrossRef][Medline]
Moore T and Fallah M. Control of eye movements and spatial attention. Proc Natl Acad Sci USA 98: 1273–1276, 2001.
Posner MI. Orienting of attention. The VIIth Sir Frederic Bartlett Lecture. Q J Exp Psychol 32: 3–25, 1980.[ISI][Medline]
Posner MI and Cohen Y. Components of visual orienting. In: Attention and Performance X, edited by Bouma H and Bouwhuis D. Hillsdale: Erlbaum, 1984, p. 531–556.
Posner MI, Rafal RD, Choate LS, and Vaughan J. Inhibition of return: neural basis and function. Cog Neuropsychol 2: 211–228, 1985.
Sapir A, Soroker N, Berger A, and Henik A. Inhibition of return in spatial attention: Direct evidence for collicular generation. Nat Neurosci 2: 1054–1054, 1999.
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