Elsevier

Brain and Cognition

Volume 53, Issue 1, October 2003, Pages 34-41
Brain and Cognition

Hemispheric asymmetries for selective attention apparent only with increased task demands in healthy participants

https://doi.org/10.1016/S0278-2626(03)00207-0Get rights and content

Abstract

This study examined the possibility that lack of behavioral evidence indicating hemispheric specialization for selective attention in healthy individuals is due to the use of tasks that are not sufficiently demanding to require selective attention. In a group of 43 participants (ages 17–23), we compared selective attention on a cued-response time task when the target was presented alone and when a distractor was simultaneously presented. The costs of invalid cueing were minimal when the right hemisphere (RH) processed the target relative to when the left hemisphere (LH) processed the target, but only for the high load condition. These results are interpreted as RH specialization in light of evidence suggesting that the RH can direct attention to a larger portion of the visual field.

Introduction

Selective attention refers to a set of mechanisms that function to limit or focus the stream of incoming information from the environment that subsequently receives more elaborate processing. This subcomponent of attentional processing has widely been studied with the cued-response time (RT) paradigm, originally designed by Posner (1980) to measure the efficiency with which covert attention (i.e., attentional movement in the absence of overt eye movements) is allocated to different regions of extrapersonal space. In a typical covert orienting experiment, the participant’s task is to make a simple response indicating the detection of a target in one or the other visual field. Prior to the onset of the target, a cue is presented that may correctly indicate the probable subsequent target location (valid cue), may falsely indicate the subsequent target location (invalid cue), or is uninformative with respect to target location (neutral cue). Typically, RT for detection of the target is faster on valid cue trials than on neutral cue trials (benefits), and slower on invalid cue trials than on neutral cue trials (costs). Posner and his colleagues have proposed that facilitation of RT at the validly cued location reflects the time savings in having already oriented to the target location based on the cue, whereas the lengthened RT to invalidly cued targets are due to the time required to disengage and reorient attention from an incorrect to a correct spatial location (Posner, 1988; Posner & Petersen, 1990).

Posner’s orienting task has also been used to assess hemispheric specialization for selective attentional processing both in brain damaged and healthy participants. In one study, patients with right hemisphere (RH) lesions were more impaired than patients with left hemisphere (LH) lesions on invalid cue trials in their ability to disengage their covert attention from the ipsilesional visual field when a target was presented in the contralesional visual field (Posner, Walker, Friedrich, & Rafal, 1984). However, the opposite pattern of results was obtained in another study with RH and LH brain-damaged patients (Petersen, Robinson, & Currie, 1989). Verfaellie, Bowers, and Heilman (1988) used the cued-RT paradigm with healthy participants but did not find any hemispheric asymmetries. Compared to a neutral cue condition, valid cues resulted in an equal reduction in RT for stimuli presented in the left visual field (LVF) and the right visual field (RVF), suggesting that both hemispheres benefited equally from the information provided by the valid cues.

Other studies have combined behavioral and physiological measures to assess hemispheric specialization for selective attentional processing. For example, consistent with Verfaellie et al. (1988), Yamaguchi, Tsuchiya, and Kobayashi (1994) found that event-related potential (ERP) activation of the LH to cues directing attention to the RVF was comparable to the activation of the RH to cues directing attention to the LVF in the early stages of attention shifts (i.e., 250 ms after cue onset). Thus, they argued that the phasic directing of attention is symmetrically organized. In another study, Corbetta, Miezin, Shulman, and Petersen (1993) measured regional cerebral blood flow changes with positron emission tomography (PET) scans in normal volunteers while they performed the cued-RT task. Similar to Verfaellie et al. (1988), they did not find any visual field asymmetries on the behavioral task. Their PET findings, however, indicated a specialized role of the RH in attentional processing. Specifically, they found that movement of attention to the LVF was primarily controlled by one region in the right parietal cortex, whereas a left parietal and a distinct right parietal region controlled movement of attention to the RVF. Thus, the RH appeared to mediate attention to both visual fields, whereas the LH could only orient attention to the right side of space (see also Kinsbourne, 1970, Kinsbourne, 1987). Other physiological studies have found evidence to support the RH’s ability to direct attention to a larger portion of the visual field (Heilman & Van Den Abell, 1980; Proverbio, Zani, Gazzaniga, & Mangun, 1994).

The lack of clear support for RH specialization for selective attentional processing on behavioral tasks is surprising given that (1) physiological studies have shown that the RH is specialized in its ability to attend to a larger portion of the visual field as compared to the LH (Corbetta et al., 1993; Heilman & Van Den Abell, 1980; Proverbio et al., 1994); (2) the RH has been found to play a more specialized role in mediating other components of attentional processing, including arousal (Benton, 1986; De Renzi & Faglioni, 1965; Heilman and Van Den Abell, 1979, Heilman and Van Den Abell, 1980; Howes & Boller, 1975; Jeeves & Dixon, 1970), sustained attention (Pardo, Fox, & Raichle, 1991; Whitehead, 1991; Yamaguchi et al., 1994), and intentional processing (Verfaellie et al., 1988; Verfaellie & Heilman, 1987); and (3) the prevalence and severity of unilateral neglect in particular (Gainotti, Messerli, & Tissot, 1972; Weintraub & Mesulam, 1989), and attentional deficits in general (e.g., Mosidze, Mkheidze, & Makashvili, 1994), are greater after RH lesions compared to LH lesions.

The current study examined the possibility that the lack of behavioral evidence indicating RH specialization for selective attention may be due to the use of tasks that are not sufficiently demanding to require specialized selective attentional processes. It may be significant that the evidence indicating that both hemispheres are equally efficient in selective attention on the behavioral tasks described above is based on findings from studies in which the target is presented alone in the visual field in the absence of competing distracting information. This situation is quite artificial, given the everyday task demands in attentional processing. The concept of selection implies that only a subset of impeding information is “selected” for further processing in the context of a highly complex and rich environment. That is, the typical environment in which selective attention operates is characterized by competition of resources resulting in an increased perceptual load. It is possible, therefore, that RH specialization for selective attention is apparent only under conditions in which the perceptual load of the task is sufficient to require the process of selection to be engaged.

Evidence to support the notion that hemispheric asymmetries may arise under conditions of competition of resources (resulting in an increased perceptual load) is provided in a study of spatial orienting in healthy adults. Using a line bisection task, Roy, Reuter-Lorenz, Roy, Copland, and Moscovitch (1987) found that when there was no orienting conflict (i.e., when the line was flanked by a box which appeared randomly either to the left or the right of the endpoint of the line), bisection accuracy was equivalent for LVF and RVF conditions. However, when there was an orienting conflict (i.e., boxes were presented in the LVF and the RVF simultaneously and participants were told to selectively attend to one or the other box while making the line bisection judgment) an asymmetry was observed. Specifically, when participants oriented to the right, they neglected the left extent of the line to a greater degree than when they oriented to the left and neglected the right extent of the line. These findings suggest that under conditions of competition of resources, the RH can outperform the LH by minimizing the degree of right neglect, and they are consistent with the notion that the RH can distribute attention more widely across space.

Additional evidence to support RH specialization for selective attentional processing under conditions of competition of resources was also recently found in a study using the pre-cueing paradigm (Evert & Oscar-Berman, 2001). A cued-detection paradigm was used in which a peripherally located cue provided information about the most probable spatial location of a subsequent target letter. The target letter appeared in either the LVF or RVF while a distractor letter was simultaneously presented in the opposing visual field. Valid, neutral, and invalid cues were used to assess whether any hemispheric differences in attentional processing were due to differences in the extent to which participants benefited from valid cues compared to neutral cues (benefits), or the extent to which they were disadvantaged by invalid cues compared to neutral cues (costs). For a group of participants (ages 26–47) the magnitude of the benefits associated with valid cues and the magnitude of the costs associated with invalid cues differed as a function of which hemisphere was activated by the peripherally located cue. Following LH activation by the cue, there was both a benefit associated with valid cues and a cost associated with invalid cues, suggesting that attention was primarily directed toward the right (cued) side of space. Following RH activation, on the other hand, performance was not only enhanced on valid cue trials, but also on invalid cue trials. This efficient processing on invalid cue trials was attributed to the RH’s ability to direct attention to a larger portion of the spatial array (Evert & Oscar-Berman, 2001). Thus, this study also supports RH specialization for selective attentional processing under conditions of competition of resources, and provides further behavioral evidence to support the RH’s ability to attend to a larger portion of the visual field than the LH.

The present experiment was designed to directly test the hypothesis that RH specialization for selective attention may be apparent only under conditions in which the perceptual load of the task is demanding enough for selection processes to be necessary for efficient performance. In a group of healthy participants, we compared the efficiency of selective attentional processing on a cued-RT task under conditions of low perceptual load (i.e., presenting the target alone in the visual field) to conditions in which there was a higher perceptual load (i.e., presenting a target in one visual field simultaneously with a distractor in the opposing visual field). Centrally located valid, neutral, and invalid cues were utilized in order to assess visual field asymmetries in the processing of LVF and RVF targets both in terms of benefits from valid cues (Neutral RT–Valid RT), as well as costs from invalid cues (Invalid RT–Neutral RT).

Because we included valid, neutral, and invalid cue trials, it was important to consider that the particular manifestation of hemispheric asymmetries for selective attentional processing could be revealed in either differential benefit effects or differential cost effects. For example, RH specialization could be manifested as larger benefits from valid cues when the RH processes the target (via LVF input) than when the LH processes the target (via RVF input). Recall that this was the operational definition used by Verfaellie et al. (1988). This finding would suggest that the RH is more efficient than the LH in selecting and maintaining attention at the cued location, and thus is more efficient in processing information in the selected spatial location.

It is also possible that hemispheric specialization for selective attention could be manifested in reduced cost effects. For example, even on invalid cue trials, targets presented to the RH (via LVF input) might be more efficiently processed than those presented to the LH (via RVF input). The results from the Evert and Oscar-Berman (2001) study might lead us to expect differential cost effects, rather than differences in the magnitude of the benefits. However, it is important to note that there were methodological differences between that study and the present one (e.g., peripheral vs. central cues; detection vs. discrimination task). Therefore, we felt that it was important to consider both possible manifestations of hemispheric asymmetries. Regardless of the exact manifestation, however, we expected that visual field asymmetries would be present only for the high perceptual load condition.

Section snippets

Participants

A total of 43 individuals (24 females, 19 males) between the ages of 17 and 23 years (mean=19, SD=1) participated in the study. They were recruited from the undergraduate population at the University of Massachusetts, Lowell campus. All participants were carefully screened to ensure that they were right-handed (forced-right handers and ambidextrous individuals were excluded), had normal or corrected-to-normal vision, and were free from neurological disease, major medical illnesses, learning

Results

Trials with incorrect responses were excluded from the RT analysis (see Table 1). In addition, trials in which RTs were more than two standard deviations from the mean within each experimental condition (outliers) for each participant were excluded from the data analysis. This procedure resulted in eliminating, on the average, 9 data points for each participant.

Two analyses were performed. For the first analysis, the mean correct RT data (reported in milliseconds) was subjected to a mixed

Discussion

The findings from the present study indicate that hemispheric asymmetries for selective attentional processing were found in cost effects from invalid cues, but not in the benefits from valid cues in a group of healthy participants. More specifically, the cost of invalid cueing on the processing of LVF targets by the RH was minimal compared to the cost of invalid cueing on the processing of RVF targets by the LH. This visual field asymmetry was present only for the condition in which a target

Acknowledgements

The research was supported by a National Research Service Award training Grant (T32 DC00017) awarded to the first author, and by an NINDS Grant (NS29342) awarded to Boston University School of Medicine. We would like to thank the Harvard Cooperative Program on Aging for referring healthy older participants and Rachel Tunick for assistance in data collection. We would also like to thank Robert Kunzendorf for testing space and participant recruitment at the University of Massachusetts at Lowell.

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