A bilateral advantage for storage in visual working memory

Abstract

Various studies have demonstrated enhanced visual processing when information is presented across both visual hemifields rather than in a single hemifield (the bilateral advantage). For example, Alvarez and Cavanagh (2005) reported that observers were able to track twice as many moving visual stimuli when the tracked items were presented bilaterally rather than unilaterally, suggesting that independent resources enable tracking in the two visual fields. Motivated by similarities in the apparent capacity and neural substrates that mediate tracking and visual working memory (WM), the present work examined whether or not a bilateral advantage also arises during storage in visual WM. Using a recall procedure to assess working memory for orientation information, we found a reliable bilateral advantage; recall error was smaller with bilateral sample displays than with unilateral displays. To demonstrate that the bilateral advantage influenced storage per se rather than just encoding efficiency, we replicated the observed bilateral advantage using sequentially presented stimuli. Finally, to further characterize how bilateral presentations enhanced storage in working memory, we measured both the number and the resolution of the stored items and found that bilateral presentations lead to an increased probability of storage, rather than enhanced mnemonic resolution. Thus, the bilateral advantage extends beyond the initial selection and encoding of visual information to influence online maintenance in visual working memory.

Introduction

The organization of the visual system is primarily contralateral such that information from the left visual hemifield is initially processed in the right hemisphere while information from the right visual hemifield is processed in the left hemisphere. Although information from these separate pathways is eventually integrated via the connecting fibers of the corpus callosum, various studies have reported enhanced performance when items are distributed across both hemifields such that both the right and left hemispheres receive the initial input, compared to when a single hemisphere processes the same amount of information. This effect has been termed the bilateral advantage. Alvarez and Cavanagh (2005) provided one of the most compelling demonstrations of a bilateral advantage using a task that required observers to simultaneously track multiple targets that were presented in either unilateral or bilateral displays. This study revealed an approximate doubling of tracking capacity when the targets were spread across both hemifields compared to when the same number of targets occupied a single hemifield, suggesting independent attentional capacities in the right and left cerebral hemispheres. The Alvarez and Cavanagh (2005) findings dovetail with several other studies that also showed a clear bilateral advantage during encoding-limited tasks that required pattern matching (Muller et al., 2003, Reuter-Lorenz et al., 1999, Sereno and Kosslyn, 1991) or rapid target discrimination (Awh and Pashler, 2000, Carlson et al., 2007, Kraft et al., 2005, Kraft et al., 2007, Liu et al., 2009, Scalf et al., 2007).

Although the tracking task employed by Alvarez and Cavanagh (2005) differed in important ways from the tasks used in other demonstrations of the bilateral advantage, they offered a hypothesis that is consistent with the full range of findings. Specifically, Alvarez and Cavanagh (2005) suggested that there may be hemisphere-specific resources that are required for the initial selection of target items, while later stages of processing such as identification and memory storage may not show hemifield independence. With the exception of split-brain patients, this hypothesis was in line with previous failures to find strong evidence of hemisphere-dependent resources in normal, healthy individuals in visual search tasks (Luck, Hillyard, Mangun, & Gazzaniga, 1989) and memory storage (Duncan et al., 1999). Thus, while Alvarez and Cavanagh (2005) provided definitive evidence of a bilateral advantage during attentive tracking, similar evidence from memory-limited tasks has been elusive (but see Delvenne, 2005). Nevertheless, there is a growing body of neural and behavioral evidence suggesting functional overlap between attentive tracking and storage in visual WM. Past studies have reported a similar capacity limit for the two such that approximately 3–4 objects can be actively maintained in visual working memory (Luck and Vogel, 1997, Pashler, 1988, Sperling, 1960, Vogel et al., 2001), and tracked simultaneously (Cavanagh and Alvarez, 2005, Oksama and Hyönä, 2004, Pylyshyn and Storm, 1988). In line with these similar capacity limits, Oksama and Hyönä (2004) found reliable correlations between an individual’s performance in MOT and visuospatial WM tasks. Likewise, Fougnie and Marois (2006) demonstrated strong dual task interference effects when subjects were required to simultaneously track objects and store items in visual WM. Finally, fMRI and ERP studies have suggested that similar neural regions mediate attentive tracking and storage in visual WM. Functional MRI studies have revealed common brain regions that are active during both MOT and VSTM tasks, including the frontal eye fields and intraparietal sulcus (Culham et al., 1998, Culham et al., 2001, Howe et al., 2009, Jovicich et al., 2001, Linden et al., 2003, Todd and Marois, 2004, Todd and Marois, 2005, Xu and Chun, 2006). More recently, Drew and Vogel (2008) recorded event-related potentials during an MOT task, and found a robust CDA (contralateral delay activity) waveform that strongly predicted individual tracking ability. The CDA waveform, whose activity is likely to arise from the intraparietal sulcus (IPS), has been previously shown to be a robust predictor of capacity in visual WM (Vogel and Machizawa, 2004, Vogel et al., 2005). A similar link between WM capacity and activity in the posterior parietal cortex was also observed by Todd and Marois (2005) in a voxelwise fMRI analysis. These results together suggest that a common neural resource may mediate performance both in the tracking and visual WM tasks, and highlight the possibility that a bilateral advantage may influence performance in both tasks.

Indeed, there is one published demonstration of a bilateral advantage during a visual working memory task. Using a standard change detection task, Delvenne (2005) measured capacity in a spatial WM task and found a reliable enhancement of capacity when the stored positions were presented bilaterally relative to when they were presented unilaterally. This result is consistent with the hypothesis that WM storage is improved in the bilateral condition, but one alternative explanation requires consideration. Given that success in the change detection task is dependent on both successful encoding and storage of the target items, the possibility remains that the bilateral advantage in the Delvenne (2005) study resulted from differences in the quality of stimulus encoding in the bilateral and unilateral conditions. Thus, a key goal of the present research was to re-examine whether WM storage is subject to a bilateral advantage while attempting to rule out stimulus encoding as the source of this putative effect. Conclusive evidence of a bilateral advantage during WM storage would show that even relatively late-stage memory processes are influenced by hemisphere-specific resource limits. To anticipate the results, our studies showed a reliable bilateral advantage during the maintenance of orientation information in visual WM. Furthermore, this bilateral advantage was robust even when the memoranda were presented sequentially, thereby precluding the possibility of a bilateral advantage during stimulus encoding. These data complement those of Delvenne (2005) by showing that storage in WM per se is enhanced when the stored items are initially presented to separate hemispheres.

Finally, we examined which aspect of memory storage was affected by the bilateral advantage. Recent evidence has suggested that WM capacity may be determined by two distinct aspects of memory ability, such that separate factors determine the maximum number of items that can be held in WM, and the precision or resolution of those memory representations (Awh et al., 2007, Barton et al., 2009, Scolari et al., 2008, Xu and Chun, 2006, Zhang and Luck, 2008). Xu and Chun (2006) provided neural evidence for this dissociation by demonstrating that activity in distinct neural regions reflected the number of items stored in working memory, and the complexity of the stored items. Given that higher resolution is needed for accurate performance with complex objects, the findings of Xu and Chun (2006) suggest that distinct neural regions mediate number and resolution in visual WM. In line with this neural dissociation, an analysis of individual differences (Awh et al., 2007) found no correlation between these two aspects of memory storage. That is, subjects who could hold a larger number of items in WM were not necessarily the same subjects who could maintain the items with higher resolution. This raises an interesting question about how bilateral presentations may affect storage in working memory. When the items to be stored are bilaterally arrayed, does this enable the storage of a larger number of items, or does it instead influence the resolution of the stored representations? To answer this question, we employed an analytic procedure developed by Zhang and Luck (2008) that enables separate estimates of the number and resolution of the representations stored in WM. This procedure replicated our findings of a reliable memory advantage in the bilateral condition. Importantly, the bilateral advantage was found only with respect to the number of items maintained in WM; the resolution of the stored representations was equivalent in the bilateral and unilateral conditions.