Research report
Event-related potentials reveal dissociable mechanisms for orienting and focusing visuospatial attention

https://doi.org/10.1016/j.cogbrainres.2004.11.014Get rights and content

Abstract

The neural mechanisms supporting visuospatial orienting and focusing were investigated by recording event-related potentials (ERPs) in a cued, line-orientation discrimination task. Search arrays flashed randomly in the left or right visual field and were preceded by peripheral cues that varied in validity (valid or invalid, with 50% each) and size (large or small, with 50% each). Facilitation of response time was observed for valid trials, regardless of cue size. In contrast to previous cued search studies, however, small (i.e., more precise) cues were associated with delayed responses. Both the timing and the amplitudes of the early ERP components, P1 and N1, were modulated by attentional orienting, with valid trials eliciting a larger and later contralateral vP1 (ventral P1) and a smaller and later contralateral N1 compared to invalid trials. Attentional focusing modulated only the amplitudes of the P1 component, with precisely cued trials eliciting a larger dP1 (dorsal P1) than less precisely cued trials at both contralateral and ipsilateral sites. Thus, both attentional orienting and focusing modulate early stimulus processing stages that overlap in time, but with dissociable effects on the scalp distribution of these components, indicating possibly different underlying mechanisms. In addition, the results support the notion that voluntary and involuntary allocations of visuospatial attention are mediated by different underlying neural processes.

Introduction

The human visual system can both orient and focus attention to a restricted region of visual space so that the perception of the stimuli within that area is facilitated [9], [27], [42]. However, the relation between these two processes is not fully understood, particularly when attention is involuntary. A processing benefit from a precue to target location – a cue validity effect – has been consistently observed. This effect shows that responses are faster and/or more accurate for valid (i.e., the target location is predicted by the cue) than for invalid trials (i.e., the target appears at an uncued location) [37], possibly because disengagement and shifting processes of visuospatial attention are involved during invalid trials, in addition to the engagement of attention in valid trials [44]. The cue validity effect can be induced by peripheral cues that draw attention involuntarily, or by central, symbolic cues which direct attention voluntarily [5], [22]. The overall effects of both types of cue on performance are similar, although their underlying mechanisms are different [45].

In addition to the ability to orient and shift attention in space, people can also adjust the size of the focus of attention. The attentional focus has been likened to a “zoom lens” [14] in which processing efficiency declines as the area to be attended increases [13]. This decline in efficiency has been termed a cue size effect of visuospatial attention in visual detection and discrimination tasks [3], [4], [49], or a scaling effect of visuospatial attention in visual search tasks [17], [18], [19]. Typical cue size or scaling effects indicate that a larger distribution or focus of attention in space slows processing relative to a smaller focus.

In the present study, we use the term “orienting” to refer to the ability to move the attentional focus in visual space, and “focusing” to refer to the ability to adjust the size of the attentional focus in the space. Furthermore, “involuntary” refers to reflexive processes elicited by peripheral cueing with a short cue-to-stimulus onset asymmetry (SOA); “voluntary” refers to the processes elicited by either central cueing or peripheral cueing with a long cue-to-stimulus SOA. According to these definitions, previous studies have revealed that the orienting of visuospatial attention, as indicated by the cue validity effect, can be elicited in both an involuntary and a voluntary manner [5], [37]. Similarly, the focusing of visuospatial attention, as indicated by the cue size effect, can also be elicited in both an involuntary ([33], [49] experiments 3 and 4) and a voluntary fashion ([17], [49] experiments 1 and 2).

Despite these similarities, there is some evidence that attentional focusing is distinct from orienting. First, focusing can take place without orienting, whereas orienting may simultaneously activate focusing [4], [49]. For example, the abrupt onset of cues can attract attention and change the focus size inside or just outside the attentional focus, without the process of orienting [49]. Second, strong focusing of attention in one visual field can inhibit orienting when the abrupt stimulus onset appears at another part of the visual field [48], [50], [54]. Third, orienting of visuospatial attention can be triggered by both stimulus onset and offset [48], whereas focusing can be triggered only by onsets but not offsets [49], suggesting that some mechanisms that trigger orienting cannot trigger focusing.

It has been suggested that the processing components of orienting and focusing of voluntary visuospatial attention are deployed independently in visual search tasks, depending on task demands [18]. However, it is unclear whether this also applies to involuntary visuospatial attention. Single-unit and brain imaging studies have shown that voluntary orienting of visuospatial attention modulates stimulus processing in extrastriate cortex [29], [36], and possibly striate cortex (for a review, see Ref. [43]). The neural regions responsible for involuntary orienting of visuospatial attention have been less well investigated using these methods. As to the focusing of visuospatial attention, a recent functional imaging study found that the magnitude of the activation in striate and extrastriate cortex increased, and the extent of the activation decreased, as the focus size constricted voluntarily [38].

The event-related potential (ERP) method provides a good tool for investigating neural events due to its millisecond-level temporal resolution. The voluntary orienting of attention facilitates visual processing by modulating the early P1 component, which reflects neural activity in extrastriate cortex, as well as the later N1 component [6], [7], [11], [23], [24], [32], [34], [39]. Involuntary orienting of attention elicited by peripheral cueing has also been found to modulate visual processing in extrastriate cortex, but with different modulations of the latency and amplitude of the P1 and N1 components [16], [26], [28], suggesting that voluntary and involuntary attentional orienting are mediated by different neural processes.

In previous work we observed that orienting of visuospatial attention elicited by peripheral cues modulated the P1 and N1 ERP components. More specifically, we found that the contralateral P1 was larger, and the contralateral N1 was smaller, for valid compared to invalid trials [16]. Meanwhile, Luo et al. provided ERP evidence of the mechanisms of attentional focusing by systematically manipulating the cue size of peripheral cues [30]. Luo et al. observed that a less precisely cued target (large cue) elicited a larger P1 and a smaller N1 than a more precisely cued target (small cue). Therefore, both attentional orienting and attentional focusing via peripheral cues have been found to elicit a larger P1 but a smaller N1 [16], [30], suggesting that these two processes are initiated at similar time points after stimulus onset and have similar ERP modulations in the early stage of processing. Thus, although the behavioral evidence reviewed above suggests that orienting and focusing of visuospatial attention are distinct processes, the psychophysiological evidence is less clear.

Using ERPs, the present study examined the underlying mechanisms of orienting and focusing of involuntary visuospatial attention and the relationship between these mechanisms. Orienting was measured as the cue validity effect elicited by peripheral location cues, whereas focusing was measured as the cue size effect arising from the manipulation of the size of the peripheral cues. We addressed three questions regarding the timing and independence of attentional orienting and focusing: (1) Can a cue size effect be elicited under experimental conditions which can elicit a peripheral cue validity effect? That is, can attentional focusing occur under the same conditions optimal for involuntary attentional orienting? (2) Can a cue validity effect be modulated by the size of peripheral cues, or can a cue size effect be modulated by the validity of the peripheral cues? That is, what is the relationship between attentional orienting and focusing? (3) Are orienting and focusing of visuospatial attention dissociable processes, or they do share the same underlying neural mechanisms? We reasoned that similar orienting-related and focusing-related ERPs point to similar underlying neural processes, whereas different ERP manifestations indicate two dissociable processes.

Section snippets

Participants

Seventeen healthy participants (9 male) participated as paid volunteers. One male participant's data were excluded from data analyses because of uncontrollable eye blinks. Participants were between 18 and 32 years of age (mean age of 24.1 years), right-handed, and had normal or corrected to normal vision. They reported no history of neurological illness. Informed consent was obtained.

Stimuli

A fixation cross (0.5° × 0.5°) was presented at the center of the monitor (black on white) throughout the whole

Behavioral measures

Participants missed 10.45% of the targets, and their mean false alarm rate was 1.16%. As shown in Fig. 2, participants responded faster to valid than to invalid targets [662 vs. 703 ms, F(1,15) = 17.444, P < 0.001]. In contrast to previous studies manipulating precue size [3], [4], [18], [19], participants responded moderately faster to the targets preceded by large cues than to those preceded by small cues [669 vs. 697 ms, F(1,15) = 14.144, P < 0.002]. No other main effects or interactions

Discussion

The present study used event-related potentials to investigate the neural mechanisms of orienting and focusing of visuospatial attention in a peripheral cueing task. More specifically, we sought to determine whether a single involuntary attentional mechanism can account for both cue validity and cue size effects, or alternatively whether these effects represent the operation of distinct cognitive and neural processes. Response time measures replicated the typical cue validity effect but

Conclusions

Orienting and focusing have been likened to “reaching and grasping” of the hand when trying to grab hold of an object [49]. This metaphor indicates that these two processes can be deployed independently at the same time, as argued by Greenwood and Parasuraman [17], [18]. The present results provide ERP evidence for this view by showing that orienting and focusing begin at roughly the same time at an early stage of visual processing. This suggests the potentially parallel orienting and focusing

Acknowledgments

This research was supported by NIH grant AG19653 to RP. Thanks to Greg Young for assistance with data collection and processing. We are grateful to Dr. George R. Mangun and three anonymous reviewers for their valuable comments on an earlier version of this manuscript. Special thanks to Dr. Durk Talsma for providing the software package for the ADJAR algorithm and for helpful suggestions.

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